Origin of spliceosomal introns and alternative splicing

Abstract

In this work we review the current knowledge on the prehistory, origins, and evolution of spliceosomal introns. First, we briefly outline the major features of the different types of introns, with particular emphasis on the nonspliceosomal self-splicing group II introns, which are widely thought to be the ancestors of spliceosomal introns. Next, we discuss the main scenarios proposed for the origin and proliferation of spliceosomal introns, an event intimately linked to eukaryogenesis. We then summarize the evidence that suggests that the last eukaryotic common ancestor (LECA) had remarkably high intron densities and many associated characteristics resembling modern intron-rich genomes. From this intron-rich LECA, the different eukaryotic lineages have taken very distinct evolutionary paths leading to profoundly diverged modern genome structures. Finally, we discuss the origins of alternative splicing and the qualitative differences in alternative splicing forms and functions across lineages.

Figure 1.

Consensus sequences of spliceosomal intron core splicing signals for (A) human major/U2 introns, (B) yeast major/U2 introns, and (C) human minor/U12 introns. The branch point (BP) adenosine is indicated by a red arrow.

Figure 2.

Steps leading to the origin and establishment of the complex spliceosomal system of LECA during eukaryogenesis (see text).

Figure 3.

Scenarios for intron evolution: shared ancestral introns versus independent gain. Hypothetical comparisons of intron positions across orthologous genes of distantly related species are shown. (A) Many introns are in homologous positions, suggesting that these introns represent ancestral introns that have been retained. (B) Lack of correspondence between intron positions in different lineages suggest that most introns have been independently gained within each lineage.

Figure 4.

Diversity of intron densities and homogeneity of splicing signals across eukaryotes. (A) Number of introns per gene (top), 1-probability (1-p) that two introns from a species share the same 5′ss (middle) or the same BP motif (bottom) for 33 species from all major eukaryotic supergroups (see color key). (B) Association between these three features: all very intron-poor species (<0.2 introns per gene) show high levels of across-intron homogeneity for 5′ss; nearly all very intron-poor species show high levels of homogeneity for BP (clusters of species inside gray ellipses). Exceptions for BP motifs (Cryptosporidium parvum and Guillardia theta NM) are indicated by asterisks. Inferred intron densities in LECA (Csurös et al. 2011) are indicated in red.