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MBE Advance Access published online on March 10, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msh120
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted February 16, 2004
© 2004 Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved.

Original Articles

The Evolutionary Gain of Spliceosomal Introns: Sequence and Phase Preferences

Wei-Gang Qiu 1, Nick Schisler 2, and Arlin Stoltzfus 3*

1 Center for Advanced Research in Biotechnology, University of Maryland Biotechnology Institute, 9600 Gudelsky Drive, Rockville, Maryland 20850, USA
2 Center for Advanced Research in Biotechnology, University of Maryland Biotechnology Institute, 9600 Gudelsky Drive, Rockville, Maryland 20850, USA; Dept. Biology, Pomona College, Claremont, CA
3 Center for Advanced Research in Biotechnology, University of Maryland Biotechnology Institute, 9600 Gudelsky Drive, Rockville, Maryland 20850, USA; Biotechnology Division, National Institute of Standards and Technology, Mail Stop 8310, Gaithersburg, Maryland, 20899-8310

* To whom correspondence should be addressed. E-mail: arlin.stoltzfus{at}nist.gov.


  Abstract

Theories regarding the evolution of spliceosomal introns differ in the extent to which the distribution of introns reflects either a formative role in the evolution of protein-coding genes, or the adventitious gain of genetic elements. Here, systematic methods are used to assess the causes of the present-day distribution of introns in 10 families of eukaryotic protein-coding genes comprising 1868 introns in 488 distinct alignment positions. The history of intron evolution inferred using a probabilistic model that allows ancestral inheritance of introns, gain of introns, and loss of introns reveals that the vast majority of introns in these eukaryotic gene families were not inherited from the most recent common ancestral genes, but were gained subsequently. Furthermore, among inferred events of intron gain that meet strict criteria of reliability, the distribution of sites of gain with respect to reading-frame phase shows a 5:3:2 ratio of phases 0, 1 and 2 (respectively), and exhibits a nucleotide preference for MAG^GT (positions -3 to +2 relative to the site of gain). The nucleotide preferences of intron gain may prove to be the ultimate cause for the phase bias. The phase bias of intron gain is sufficient to account quantitatively for the well known 5:3:2 bias in phase frequencies among extant introns, a conclusion that holds even when taxonomic heterogeneity in phase patterns is considered. Thus, intron gain accounts for the vast majority of extant introns, and for the bias toward phase 0 introns that previously was interpreted as evidence for ancient formative introns.

Key Words: intron gain, evolution, intron phase, proto-splice site, target site


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