Large-scale comparison of intron positions among animal, plant, and fungal genes

Abstract

We purge large databases of animal, plant, and fungal intron-containing genes to a 20% similarity level and then identify the most similar animal-plant, animal-fungal, and plant-fungal protein pairs. We identify the introns in each BLAST 2.0 alignment and score matched intron positions and slid (near-matched, within six nucleotides) intron positions automatically. Overall we find that 10% of the animal introns match plant positions, and a further 7% are "slides." Fifteen percent of fungal introns match animal positions, and 13% match plant positions. Furthermore, the number of alignments with high numbers of matches deviates greatly from the Poisson expectation. The 30 animal-plant alignments with the highest matches (for which 44% of animal introns match plant positions) when aligned with fungal genes are also highly enriched for triple matches: 39% of the fungal introns match both animal and plant positions. This is strong evidence for ancestral introns predating the animal-plant-fungal divergence, and in complete opposition to any expectations based on random insertion. In examining the slid introns, we show that at least half are caused by imperfections in the alignments, and are most likely to be actual matches at common positions. Thus, our final estimates are that approximately equal 14% of animal introns match plant positions, and that approximately equal 17-18% of fungal introns match animal or plant positions, all of these being likely to be ancestral in the eukaryotes.

Fig 1.

Comparison of the animal–plant matches to the Poisson expectation. The diamonds show the number of alignments at each set of matches. The lower curve, with the squares, is the Poisson estimate fitted to the zero and single hit numbers.

Fig 2.

BLAST 2.0 alignment of the RAN-binding protein. The upper sequence is the Mus musculus MMU278435 gene; the lower sequence is the Arabidopsis thaliana ATF17J16 gene. (A) The positions of common introns on the protein sequences are marked in red, sliding introns are marked in blue, and unique introns are marked in yellow. The phases of animal introns are shown above their marked positions and the phases of plant introns are shown below. The position and phase of one mapped fungal intron is shown below the aligned sequence on the green background; the digit followed by “f” indicates the phase of the fungal intron. (B and C) Segments of the alignment containing sliding intron positions are followed by the corrections to the alignment that transform sliding intron positions to common positions.