Origin and Evolution of Introns

Alexei Fedorov

    Department of Medicine, Medical College of Ohio, Toledo, Ohio 

Introns are integral elements of eukaryotic genomes that perform various
important functions and actively participate in gene evolution.  At
least six distinct roles of spliceosomal introns could be assigned: 1)
sources of non-coding RNA; 2) carriers of transcription regulatory
elements; 3) actors in alternative and trans-splicing; 4) enhancers of
meiotic crossing over within coding sequences; 5) substrates for exon
shuffling; and 6) signals for mRNA export from the nucleus and
nonsense-mediated decay. In the late 1970’s, Francis Crick and others
suggested that new introns might arise as transposons that either come
equipped with or quickly acquire signals sufficient for splicing.
However, the mechanism of acquisition has yet to be described for a
single animal intron.  We performed a large-scale computational analysis
of the human, D. melanogaster, C. elegans, and A. thaliana genomes.
147,796 human intron sequences were divided into batches of similar
lengths and aligned with each other.  Different types of homologies
between introns were found, but none showed evidence of simple intron
transposition. Also, 106,902 plant, 39,624 Drosophila and 6,021 C.
elegans introns were examined. No single case of homologous introns in
non-homologous genes was detected.  Thus we found no example of
transposition of introns in the last 50 million years in humans, in 3
million years in Drosophila and C. elegans, or in 5 million years in
Arabidopsis.  Either new introns do not arise via transposition of other
introns or intron transposition must have occurred so early in evolution
that all traces of homology have been lost. 

We also explored possible peculiarities of intron structures at the
earliest stage of evolution, known as an RNA world. These peculiarities,
which existed in the absence of DNA, shed light on introns’ original
functions as well as the important role they played in the origin of
life. We propose that introns and other non-coding segments of nucleic
acids could be mighty functional elements governing the fate of RNA and
DNA molecules in RNA-protein world, as well as more advanced species.