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The Highly Conserved Family of Tetrahymena thermophila Chromosome Breakage Elements Contains an Invariant 10-Base-Pair Core

Eileen P. Hamilton,^* Sondra Williamson, Sandra Dunn, Virginia Merriam,^# Cindy Lin, Linh Vong,^¶ Jessica Russell-Colantonio,^|| and Eduardo Orias

Department of Molecular, Cellular and Developmental Biology, University of California at Santa Barbara, Santa Barbara, California 93106

Received 28 October 2005/ Accepted 12 January 2006

As a typical ciliate, Tetrahymena thermophila is a unicellular eukaryote that exhibits nuclear dimorphism: each cell contains a diploid, germ line micronucleus (MICN) and a polyploid, somatic macronucleus (MACN). During conjugation, when a new MACN differentiates from a mitotic descendant of the diploid fertilization nucleus, the five MICN chromosomes are site-specifically fragmented into 250 to 300 MACN chromosomes. The classic chromosome breakage sequence (CBS) is a 15-bp element (TAAACCAACCTCTTT) reported to be necessary and sufficient for chromosome breakage. To determine whether a CBS is present at every site of chromosome fragmentation and to assess the range of sequence variation tolerated, 31 CBSs were isolated without preconception as to the sequence of the chromosome breakage element. Additional CBS-related sequences were identified in the whole-genome sequence by their similarities to the classic CBS. Forty CBS elements behaved as authentic chromosome breakage sites. The CBS nucleotide sequence is more diverse than previously thought: nearly half of the CBS elements identified by unbiased methods have a variant of the classic CBS. Only an internal 10-bp core is completely conserved, but the entire 15-bp chromosome breakage sequence shows significant sequence conservation. Our results suggest that any one member of the CBS family provides a necessary and sufficient cis element for chromosome breakage. No chromosome breakage element totally unrelated to the classic CBS element was found; such elements, if they exist at all, must be rare.

Supplemental material for this article may be found at http://ec.asm.org/.

Present address: Microbiology and Immunology H107, Penn State College of Medicine, 500 University Drive, Hershey, PA 17033.

^# Present address: Department of Biology, Loyola Marymount University, Los Angeles, CA 90045.

Present address: Gen-Probe, 10210 Genetic Center Drive, San Diego, CA 92121.

^¶ Present address: Department of Medicine and Division of Endocrinology, Diabetes, and Metabolism, Beth Israel Deaconess Medical Center, and Harvard Medical School, Boston, MA 02115.

^|| Present address: MIMG, University of California, Los Angeles, CA 90095.

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