Birth of new spliceosomal introns in fungi by multiplication of introner-like elements

Abstract

Spliceosomal introns are noncoding sequences that separate exons in eukaryotic genes and are removed from pre-messenger RNAs by the splicing machinery. Their origin has remained a mystery in biology since their discovery because intron gains seem to be infrequent in many eukaryotic lineages. Although a few recent intron gains have been reported, none of the proposed gain mechanisms can convincingly explain the high number of introns in present-day eukaryotic genomes. Here we report on particular spliceosomal introns that share high sequence similarity and are reminiscent of introner elements. These elements multiplied in unrelated genes of six fungal genomes and account for the vast majority of intron gains in these fungal species. Such introner-like elements (ILEs) contain all typical characteristics of regular spliceosomal introns (RSIs) but are longer and predicted to harbor more stable secondary structures. However, dating of multiplication events showed that they degenerate in sequence and length within 100,000 years to eventually become indistinguishable from RSIs. We suggest that ILEs not only account for intron gains in six fungi but also in ancestral eukaryotes to give rise to most RSIs by a yet unknown multiplication mechanism.