Evolution of eukaryotic gene structure: remarkable conservation of intron positions in plants and vertebrates and massive, lineage-specific loss of introns
Eugene
V. Koonin
National
Center for Biotechnology Information, National Library of Medicine, National
Institutes of Health, Bethesda MD, USA
Most
of the eukaryotic protein-coding genes contain multiple introns that are
spliced out of the pre-mRNA by a distinct, large RNA-protein complex, the
spliceosome, which is conserved throughout the eukaryotic world. Anecdotal
observations indicate that positions of some introns are conserved in
orthologous genes from plants and animals. However, intron densities in
different eukaryotic species differ widely and the location of introns in
orthologous genes does not always coincide even in closely related species, and
likely cases of intron insertion and loss have been documented. Thus, both
intron loss and intron insertion clearly occur in eukaryotic evolution. It has
been suggested that the proportion of shared intron positions decreased with
increasing evolutionary distance, which potentially could make intron
conservation a useful phylogenetic marker. However, evolutionary history of
introns and the selective forces that shape intron evolution remain major mysteries.
In particular, it is unclear whether the genome of the common ancestor of
animals, plants and fungi was intron-rich or intron-poor, how many ancestral
introns are retained in extant genomes and what are the relative contributions
of intron loss and intron insertion in the evolution of eukaryotic genes. We
addressed this problem taking advantage of the recently constructed collection
of clusters of orthologous eukaryotic genes (COGs). Intron positions were
analyzed in 1181 orthologous gene sets from six
completely sequenced genomes of animals, plants and fungi and constructed
parsimonious scenarios of evolution of the exon-intron structure for the
respective genes. Paradoxically, humans share substantially more introns with
the plant Arabidopsis thaliana than with fly or nematode. This is
explained by postulating the presence of numerous introns in the common
ancestor of animals, plants and fungi. Many of these ancestral introns are
conserved in vertebrates and plants, in which they comprise up to 25% of all
introns, but have been lost in fungi, nematodes and arthropods.