Abstract

BackgroundThe origin of spliceosomal introns is the central subject of the introns-early versus introns-late debate. The distribution of intron phases is non-uniform, with an excess of phase-0 introns. Introns-early explains this by speculating that a fraction of present-day introns were present between minigenes in the progenote and therefore must lie in phase-0. In contrast, introns-late predicts that the nonuniformity of intron phase distribution reflects the nonrandomness of intron insertions.ResultsIn this paper, we tested the two theories using analyses of intron phase distribution. We inferred the evolution of intron phase distribution from a dataset of 684 gene orthologs from seven eukaryotes using a maximum likelihood method. We also tested whether the observed intron phase distributions from 10 eukaryotes can be explained by intron insertions on a genome-wide scale. In contrast to the prediction of introns-early, the inferred evolution of intron phase distribution showed that the proportion of phase-0 introns increased over evolution. Consistent with introns-late, the observed intron phase distributions matched those predicted by an intron insertion model quite well.ConclusionOur results strongly support the introns-late hypothesis of the origin of spliceosomal introns.

Highlights

  • The origin of spliceosomal introns is the central subject of the introns-early versus introns-late debate

  • Our results strongly support the introns-late hypothesis of the origin of spliceosomal introns

  • Our result for the evolution of intron phase distribution suggests that the nonuniformity of intron phase distribution is more likely to be due to the nonrandomness of intron insertions

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Summary

Introduction

The origin of spliceosomal introns is the central subject of the introns-early versus introns-late debate. Introns-early explains this by speculating that a fraction of present-day introns were present between minigenes in the progenote and must lie in phase-0. The origin of spliceosomal introns – "extra" DNA sequences that disrupt the coding regions in nuclear genes of eukaryotes – is still a mystery. The intronsearly theory proposes that introns already existed at the progenote (i.e., the last common ancestor of prokaryotes and eukaryotes) to facilitate the construction of the first genes [1,2,3,4]. The introns-late theory, on the other hand, holds that genes at the progenote were intronless, similar to those in present-day prokaryotes, and introns were gained late, after the emergence of eukaryotes [5,6,7]. There has been no decisive resolution to the debate, and each of these theories has supporting arguments that have not been satisfactorily disproved

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