Mechanisms of intron gain and loss in Drosophila

Abstract

BackgroundIt is widely accepted that orthologous genes have lost or gained introns throughout evolution. However, the specific mechanisms that generate these changes have proved elusive. Introns are known to affect nearly every level of gene expression. Therefore, understanding their mechanism of evolution after their initial fixation in eukaryotes is pertinent to understanding the means by which organisms develop greater regulation and complexity.ResultsTo investigate possible mechanisms of intron gain and loss, we identified 189 intron gain and 297 intron loss events among 11 Drosophila species. We then investigated these events for signatures of previously proposed mechanisms of intron gain and loss. This work constitutes the first comprehensive study into the specific mechanisms that may generate intron gains and losses in Drosophila. We report evidence of intron gain via transposon insertion; the first intron loss that may have occurred via non-homologous end joining; intron gains via the repair of a double strand break; evidence of intron sliding; and evidence that internal or 5' introns may not frequently be deleted via the self-priming of reverse transcription during mRNA-mediated intron loss. Our data also suggest that the transcription process may promote or result in intron gain.ConclusionOur findings support the occurrence of intron gain via transposon insertion, repair of double strand breaks, as well as intron loss via non-homologous end joining. Furthermore, our data suggest that intron gain may be enabled by or due to transcription, and we shed further light on the exact mechanism of mRNA-mediated intron loss.

Higher frequency of intron loss from the promoter proximally paused genes ofDrosophila melanogaster

“…In mammals and Drosophila, intron losses have been found to occur preferentially in highly expressed genes. 6,9 Researchers have suggested that this supports a reverse transcriptase model of intron loss. 15 The reverse transcriptase model is an entirely different model that attempt to explain the pattern of intron loss at mutation level.…”

“…[1][2][3][4][5][6][7][8][9][10] However, it is not clear whether these intron losses occur by chance or are driven by selective forces. In principle, intron loss can be positively selected if the existence of that intron is deleterious to the host organism or if its detriments overwhelm its benefits.…”

Probing the Boundaries of Orthology: The Unanticipated Rapid Evolution ofDrosophila centrosomin

“…Relative to the dipterans, Cnn is encoded by more exons in all species investigated here with a trend toward exon fusion in the dipterans. The most common mechanism for intron loss is mediated by reverse transcriptase (Coulombe-Huntington and Majewski 2007;Yenerall et al 2011), but our results suggest that cnn introns are lost by genomic deletions (Llopart et al 2002;Yenerall et al 2011). Our comparison of the exon structure of cnn orthologs shows a potential intermediate step in this process, especially within the hymenopterans.…”

“…Protein alignments between all the species in this study suggest that the short sequences flanking fusion points are divergent between orders and continue to evolve rapidly after the fusion event within orders. Global analyses of Drosophila have shown that most introns are lost by a reverse transcriptase mechanism, resulting in the perfect excision of the intron (Coulombe-Huntington and Majewski 2007; Yenerall et al 2011). A rare second mechanism of intron loss in Drosophila is precise and imprecise genomic deletion by nonhomologous end joining (NHEJ) during DNA break repair (Llopart et al 2002;Yenerall et al 2011).…”

“…Initially, intronic deletions bring multiple exons into close proximity with each other, forming exon islands. These data do not resolve how multiple exons fuse, but imprecise NHEJ repair (Llopart et al 2002;Yenerall et al 2011) or intronic deletions resulting in intron retention (Talerico and Berget 1994) are plausible mechanisms. These two mechanisms, as well as the loss of coding exons in the lepidopterans and the incorporation of nonhomologous coding sequence in T. castaneum, would account for some of the divergence of Cnn-PA proteins.…”