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The evolution of spliceosomal introns: patterns, puzzles and progress

Key Points

  • Recent studies have uncovered the extent and pattern of conservation of intron position across widely diverged eukaryotic species.

  • Introns that are found in the genomes of modern species are mainly fairly old, with significant fractions dating to relatively deep eukaryotic ancestors.

  • Conservation of spliceosomal components across diverse eukaryotic lineages suggests the presence of a complex spliceosome in the ancestor of all extant eukaryotes.

  • This pattern of conservation might indicate that introns were already numerous in early eukaryotes, with diverse eukaryotic lineages having subsequently experienced more intron loss than gain, although debate is ongoing.

  • Analysis of apparent cases of intron loss indicates that such loss might occur through recombination between the genomic copy of the gene and a reverse transcript of a spliced mRNA copy of the gene.

  • Analysis of introns that seem to have been gained over the past 10–100 million years indicates that the new introns could arise as transposon insertions into contiguous coding sequence, not by transposition of previous introns, which was the previously favoured model.

  • Previous proposals for the causes of the vast differences between numbers of introns between eukaryotic species, which were based on inter-specific differences in either the selective value of introns or population size, have trouble explaining the apparently large numbers of introns in fairly deep eukaryotic ancestors. We propose that many of these intron-number differences could be explained by intron-loss rates.

Abstract

The origins and importance of spliceosomal introns comprise one of the longest-abiding mysteries of molecular evolution. Considerable debate remains over several aspects of the evolution of spliceosomal introns, including the timing of intron origin and proliferation, the mechanisms by which introns are lost and gained, and the forces that have shaped intron evolution. Recent important progress has been made in each of these areas. Patterns of intron-position correspondence between widely diverged eukaryotic species have provided insights into the origins of the vast differences in intron number between eukaryotic species, and studies of specific cases of intron loss and gain have led to progress in understanding the underlying molecular mechanisms and the forces that control intron evolution.

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Figure 1: Distribution of spliceosomal introns in eukaryotic species.
Figure 2: Intron conservation, gain and loss for 684 sets of eukaryotic orthologues.
Figure 3: Models and examples of intron loss.
Figure 4: Models and examples of intron gain.
Figure 5: Strange patterns of intron loss and gain.

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Correspondence to Scott William Roy.

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Saccharomyces Genome Database

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Glossary

Nonsense-mediated decay

A mechanism by which a stop codon that is encountered by the ribosome upstream of an intron–exon boundary leads to degradation of the transcript.

Exon shuffling

A process by which ectopic recombination within introns leads to the creation of new genetic products.

Dollo parsimony

A method in which a character (in this case an intron position) is inferred to have arisen exactly once on the evolutionary tree in the ancestor of the most distantly related pair of species that share the character. Absence of the character in descendents of this ancestor is then explained by the minimal pattern of losses necessary to explain the observed phylogenetic distribution.

Maximum likelihood analysis

A statistical method that finds the maximum of the likelihood function given a set of data, where the likelihood function gives the probability of obtaining the data for a set of unknown variables.

Protosplice sites

A consensus motif into which newly inserted introns seem to insert (or at least in which they are found), which is generally thought to be a variant of MAG|GT, where M denotes an A or C, and the line indicates the point of insertion.

Gene conversion

Any process by which a genomic element changes to the sequence of a paralogous element; this probably takes place mainly by double recombination.

Fixation

With respect to a given mutant, the condition in which all alleles in the population are descendents of that mutant.

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William Roy, S., Gilbert, W. The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7, 211–221 (2006). https://doi.org/10.1038/nrg1807

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