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doi:10.1534/genetics.104.039701
A more recent version of this article appeared on June 1, 2005.
REGULAR RESEARCH PAPERS |
Subdivision of Large Introns in Drosophila by Recursive Splicing at Non-exonic Elements
James M. Burnette 1, Etsuko Miyamoto-Sato 2, Marc A. Schaub 1, Jamie Conklin 1 and A. Javier Lopez 1*
1 Carnegie Mellon University
2 Yokohama National University
* To whom correspondence should be addressed. E-mail: jlaa{at}andrew.cmu.edu.
Submitted on December 13, 2004
Revised on February 8, 2005
Accepted on 8 February 2005
Many genes with important roles in development and disease contain exceptionally long introns, but the possible existence of special mechanims for their expression has not been investigated. We present bioinformatic, phylogenetic and experimental evidence in Drosophila for a general mechanism that subdivides many large introns by recursive splicing at non-exonic elements and alternative exons. Recursive splice sites predicted with highly stringent criteria are found at much higher frequency than expected in the sense strands of introns longer than 20 kb, but they are found only at the expected frequency on the antisense strands, and they are underrepresented within introns shorter than 10 kb. The predicted sites in long introns are highly conserved between Drosophila melanogaster and Drosophila pseudoobscura, despite extensive divergence of other sequences within the same introns. These patterns of enrichment and conservation suggest that recursive splice sites are advantageous in the context of long introns. Experimental analyses of in vivo processing intermediates and lariat products from four large introns in the unrelated genes kuzbanian, outspread and Ultrabithorax confirmed that these introns are removed by a series of recursive splicing steps using the predicted non-exonic sites. Mutation of non-exonic site RP3 within Ultrabithorax also confirmed that recursive splicing is the predominant processing pathway even with a shortened version of the intron. We discuss currently known and potential roles for recursive splicing in long introns.
Key Words: alternative splicing, gene structure, hybrid splice site, intron evolution, recursive splice site
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