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MBE Advance Access published online on May 23, 2007

Molecular Biology and Evolution, doi:10.1093/molbev/msm102
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Article

Widespread Intron Loss Suggests Retrotransposon Activity in Ancient Apicomplexans

Scott William Roy and David Penny

Allan Wilson Centre for Molecular Ecology and Evolution Massey University Palmerston North, New Zealand

scottwroy{at}gmail.com +64 6 350 5515 x7626 (phone) +64 6 350 5626 (fax)

Received for publication March 19, 2007. Revision received April 25, 2007. Accepted for publication May 17, 2007.

Several facets of spliceosomal intron in apicomplexans remain mysterious. First, intron numbers vary across species by two orders of magnitude, indicating massive intron loss and/or gain. Second, previous studies have shown very different evolutionary patterns over different timescales, with 100-fold higher rates of intron loss/gain between genera than within genera. Third, the timing and dynamics of near complete intron loss in Cryptosporidium species, as well as reasons for retention of the few remaining introns, remain unknown. We compared intron positions in 785 orthologous genes between three moderate to intron-rich apicomplexan species. We estimate that the Theileria-Plasmodium ancestor had 4.5 times as many introns as modern Plasmodium species and 38% more than modern Theileria species, and that subsequent intron losses have outnumbered intron gains by 5.8-to-1 in Theileria and by some 56-to-1 in Plasmodium. Several patterns suggest that these intron losses occurred by recombination with reverse transcribed mRNAs. Intriguingly, this finding suggests significant retrotransposon activity in the lineages leading to both Theileria and Plasmodium, in contrast to the dearth of known retrotransposons and intron loss within modern species from both genera. We also compared genomes from Cryptosporidium parvum and C. hominis, and found no evidence of ongoing intron loss, nor of intron gain. By contrast, Cryptosporidium introns are less evolutionary conserved with Toxoplasma than are introns from other apicomplexans, thus the few remaining introns are not simply indispensable ancestral introns.

Key Words: intron loss • intron gain • genome evolution • retrotransposon evolution • selfish DNA


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