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Abstract
BackgroundThe timing of the origin of introns is of crucial importance for an understanding of early genome architecture. The Exon theory of genes proposed a role for introns in the formation of multi-exon proteins by exon shuffling and predicts the presence of conserved splice sites in ancient genes. In this study, large-scale analysis of potential conserved splice sites was performed using an intron-exon database (ExInt) derived from GenBank.ResultsA set of conserved intron positions was found by matching identical splice sites sequences from distantly-related eukaryotic kingdoms. Most amino acid sequences with conserved introns were homologous to consensus sequences of functional domains from conserved proteins including kinases, phosphatases, small GTPases, transporters and matrix proteins. These included ancient proteins that originated before the eukaryote-prokaryote split, for instance the catalytic domain of protein phosphatase 2A where a total of eleven conserved introns were found. Using an experimental setup in which the relation between a splice site and the ancientness of its surrounding sequence could be studied, it was found that the presence of an intron was positively correlated to the ancientness of its surrounding sequence. Intron phase conservation was linked to the conservation of the gene sequence and not to the splice site sequence itself. However, no apparent differences in phase distribution were found between introns in conserved versus non-conserved sequences.ConclusionThe data confirm an origin of introns deep in the eukaryotic branch and is in concordance with the presence of introns in the first functional protein modules in an 'Exon theory of genes' scenario. A model is proposed in which shuffling of primordial short exonic sequences led to the formation of the first functional protein modules, in line with hypotheses that see the formation of introns integral to the origins of genome evolution.ReviewersThis article was reviewed by Scott Roy (nominated by Anthony Poole), Sandro de Souza (nominated by Manyuan Long), and Gáspár Jékely.
Highlights
The timing of the origin of introns is of crucial importance for an understanding of early genome architecture
A set of potential ancient splice sites An experimental set-up was defined that allowed for a systematic search for potential conserved splice sites in a genomic intron-exon database derived from GenBank (ExInt; [37])
A conserved splice site was defined as an amino acid sequence that has the same intron position and splice site sequence in two distantly-related protein sequences (Fig. 1A)
Summary
The timing of the origin of introns is of crucial importance for an understanding of early genome architecture. The question about the origin of introns is fundamental for an understanding of the evolution of the genome. Biology Direct 2007, 2:7 http://www.biology-direct.com/content/2/1/7 theory has been modified to include the insertion of introns later in evolution, while maintaining the role of early introns in creating protein diversity [12,13,14]. Proponents of both introns-early and introns-late agree that spliceosomal introns and the spliceosome already existed in the most recent common ancestor of living eukaryotes [15]. Introns-first hypotheses have been proposed that do not assume intron insertion, but trace introns to the very early origins of the genome [16,17,18], and position the origin of the spliceosome directly to the first generation of multiexon genes
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