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MBE Advance Access published online on April 13, 2005

Molecular Biology and Evolution, doi:10.1093/molbev/msi147
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© The Author 2005. 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@oupjournals.org
Accepted March 29, 2005

Research Article

An Alien Promoter Capture as a Primary Step of the Evolution of Testes-Expressed Repeats in the Drosophila melanogaster Genome

Lev A. Usakin 1, Galina L. Kogan 1, Alla I. Kalmykova 1, and Vladimir A. Gvozdev 1*

1 Department of Animal Molecular Genetics, Institute of Molecular Genetics, Moscow 123182, Kurchatov sq 2, Russia

* To whom correspondence should be addressed.
Vladimir A. Gvozdev, E-mail: gvozdev{at}img.ras.ru


   Abstract

Fertility of Drosophila melanogaster males is impaired due to the disruption of the silencing of the X-linked, testis-expressed, repeated Stellate genes. Stellate silencing is mediated by symmetric transcription of the paralogous Y-linked repeats and exerted by an RNAi mechanism. Here we present a scenario for the origin of the Stellate genes and their suppressors. The primary intermediate of their evolution emerged as a result of the acquisition of a preformed alien testis-specific promoter. This intermediate is identified as a chimeric gene containing coding region of an autosomal gene for testis-specific protein kinase CK2. The 5' region of the chimera has been acquired from a member of a family of testis-expressed X-linked genes of unknown function. We propose that the evolution and amplification of the novel chimeric gene have led to the overproduction of the regulatory CK2 subunit in testes. The evolution of the Y-linked descendants of the primary intermediate resulted in the RNAi-mediated suppression of excessive expression of the X-linked paralogs. The newly detected "dead family" of cognate repeats on the Y chromosome has contributed to the evolution of Stellate and its suppressors via gene conversion. Our results show that RNAi silencing, considered as a defense against viruses and transposable elements, may be involved in the evolution of eukaryotic genomes.

Keywords: evolution; novel gene formation; RNAi; heterochromatin; Drosophila.
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