An alien promoter capture as a primary step of the evolution of testes-expressed repeats in the Drosophila melanogaster genome.
Fertility of Drosophila melanogaster males is impaired due to the disruption of the silencing of the X-linked, testis-expressed, repeated Stellate (Ste) genes. Ste silencing is mediated by symmetric transcription of the paralogous Y-linked repeats and exerted by an RNA interference (RNAi) mechanism. Here we present a scenario for the origin of the Ste 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 Ste 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.
Usakin
Lev A
LA
Department of Animal Molecular Genetics, Institute of Molecular Genetics, Moscow, Russia.
Kogan
Galina L
GL
Kalmykova
Alla I
AI
Gvozdev
Vladimir A
VA
D000818:Animals; D001483:Base Sequence; D004251:DNA Transposable Elements; D029721:Drosophila Proteins / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics*; D019143:Evolution, Molecular; D020868:Gene Silencing; D017930:Genes, Reporter; D016678:Genome; D015151:Immunoblotting; D008297:Male; D008969:Molecular Sequence Data; D011401:Promoter Regions, Genetic; D011494:Protein Kinases / Q000235:genetics*; D034622:RNA Interference; D012091:Repetitive Sequences, Nucleic Acid; D012689:Sequence Homology, Nucleic Acid; D013489:Suppression, Genetic; D020080:Tandem Repeat Sequences; D014998:Y Chromosome
D004251:DNA Transposable Elements; D029721:Drosophila Proteins; D011494:Protein Kinases; C094331:Ste protein, Drosophila