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Originally published as Genetics Published Articles Ahead of Print on April 30, 2006.
Genetics, Vol. 173, 1433-1445, July 2006, Copyright © 2006
doi:10.1534/genetics.106.056069
Heterochromatic Genes in Drosophila: A Comparative Analysis of Two Genes
Sandra R. Schulze*,1,
Bryant F. McAllister
,
Donald A. R. Sinclair*,
Kathleen A. Fitzpatrick*,
Marcella Marchetti
,
Sergio Pimpinelli and
Barry M. Honda*,2
* Department of Molecular Biology and Biochemistry, Simon Fraser University, Burnaby, British Columbia V5A 1S6, Canada, Department of Biological Sciences, University of Iowa, Iowa City, Iowa 52242 and Istituto Pasteur, Fondazione Cenci Bolognetti and Dipartimento di Genetica e Biologia Molecolare, Università "La Sapienza," 00185 Roma, Italy
2 Corresponding author: Department of Molecular Biology and Biochemistry, Simon Fraser University, 8888 University Dr., Burnaby, BC V5A 1S6, Canada.
Centromeric heterochromatin comprises 
30% of the Drosophila melanogaster genome, forming a transcriptionally repressive environment that silences euchromatic genes juxtaposed nearby. Surprisingly, there are genes naturally resident in heterochromatin, which appear to require this environment for optimal activity. Here we report an evolutionary analysis of two genes, Dbp80 and RpL15, which are adjacent in proximal 3L heterochromatin of D. melanogaster. DmDbp80 is typical of previously described heterochromatic genes: large, with repetitive sequences in its many introns. In contrast, DmRpL15 is uncharacteristically small. The orthologs of these genes were examined in D. pseudoobscura and D. virilis. In situ hybridization and whole-genome assembly analysis show that these genes are adjacent, but not centromeric in the genome of D. pseudoobscura, while they are located on different chromosomal elements in D. virilis. Dbp80 gene organization differs dramatically among these species, while RpL15 structure is conserved. A bioinformatic analysis in five additional Drosophila species demonstrates active repositioning of these genes both within and between chromosomal elements. This study shows that Dbp80 and RpL15 can function in contrasting chromatin contexts on an evolutionary timescale. The complex history of these genes also provides unique insight into the dynamic nature of genome evolution.
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