Molecular aspects of intron evolution in dynein encoding mega-genes on the heterochromatic Y chromosome of Drosophila...

Fertility genes on the heterochromatic Y chromosome of various Drosophila species are unique for several reasons. Most of them are megabase-sized. Their expression is restricted to premeiotic spermatocytes and often associated with unfolding of huge species-specific lampbrush loops. Molecular analysis of the orthologous dynein genes Dhc-Yh3, DhDhc7(Y) and DeDhc7(Y) on the Y chromosome of the three species D. melanogaster, D. hydei and D. eohydei, respectively, revealed that the megabase gene size as well as the species-specific morphology of the corresponding lampbrush loops kl-5, Threads and diffuse loops result from huge introns and their specific sequence composition, whereas the majority of all 20 introns in each of the three genes is in a size of 45-72 bp. The loop-specifying introns are extreme exceptions due to extended assemblies of degenerated transposable elements and/or large clusters of satellite DNAs. Here we use sequence information from the complete intron sets of three orthologous Y chromosomal dynein genes to deduce a scenario for an evolutionary pathway leading to the megabase-sized genes on the heterochromatic Y chromosome of Drosophila. The obvious bias between very small and species-specific mega introns is explained as the result of an autocatalytic mode of intron growth. An initial coincidental hit by a single transposable element extends the size of a 50 bp intron for about two orders of magnitude and determines it for preferential extension by similar insertion events. This phase of continuous moderate growth is followed by rapid size enlargements by repeating amplifications generating extended clusters of satellite DNA. Size control by recombination, on the other hand, is suppressed in Drosophila males by achiasmatic meiosis.