Abstract
The alignment between the boundaries of protein domains and the boundaries of exons could provide evidence for the evolution of proteins via domain shuffling, but literature in the field has so far struggled to conclusively show this. Here, on larger data sets than previously possible, we do finally show that this phenomenon is indisputably found widely across the eukaryotic tree. In contrast, the alignment between exons and the boundaries of intrinsically disordered regions of proteins is not a general property of eukaryotes. Most interesting of all is the discovery that domain–exon alignment is much more common in recently evolved protein sequences than older ones.
Highlights
In 1978, Walter Gilbert asked: ‘Why genes in pieces?’ [1]
For 88 eukaryote genomes, we counted the number of exon boundaries that, when mapped to protein sequence positions, are within one residue of the start or end of a SUPERFAMILY structural domain assignment or a D2P2 disorder assignment
We have shown that the boundaries of exons align with the boundaries of domains more than expected by chance and that this effect is stronger in recently evolved proteins. This is found to be a consistent property of eukaryotic genomes and provides strong evidence that exon shuffling has played some role in the evolution of novel domain architectures throughout eukarya
Summary
In 1978, Walter Gilbert asked: ‘Why genes in pieces?’ [1]. This question was posed shortly after the discovery of the intron–exon architecture of eukaryotic genes. It was hypothesized that exons should correspond to some unit of protein sequence, allowing rapid evolution of new proteins and new functions through the shuffling of exons [1,2]. Evidence of this were limited and contradictory, with example followed by counterexample. More recent large-scale studies have found some support for the idea, by examining exon shuffling in the context of domains––which are units of proteins that can evolve, fold and function independently. Since alternatively spliced exons show enrichment for protein disorder [11,12,13], a correspondence between exon boundaries and regions of disorder may be expected
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