Three distinct modes of intron dynamics in the evolution of eukaryotes

Abstract

Several contrasting scenarios have been proposed for the origin and evolution of spliceosomal introns, a hallmark of eukaryotic genes. A comprehensive probabilistic model to obtain a definitive reconstruction of intron evolution was developed and applied to 391 sets of conserved genes from 19 eukaryotic species. It is inferred that a relatively high intron density was reached early, i.e., the last common ancestor of eukaryotes contained >2.15 introns/kilobase, and the last common ancestor of multicellular life forms harbored approximately 3.4 introns/kilobase, a greater intron density than in most of the extant fungi and in some animals. The rates of intron gain and intron loss appear to have been dropping during the last approximately 1.3 billion years, with the decline in the gain rate being much steeper. Eukaryotic lineages exhibit three distinct modes of evolution of the intron-exon structure. The primary, balanced mode, apparently, operates in all lineages. In this mode, intron gain and loss are strongly and positively correlated, in contrast to previous reports on inverse correlation between these processes. The second mode involves an elevated rate of intron loss and is prevalent in several lineages, such as fungi and insects. The third mode, characterized by elevated rate of intron gain, is seen only in deep branches of the tree, indicating that bursts of intron invasion occurred at key points in eukaryotic evolution, such as the origin of animals. Intron dynamics could depend on multiple mechanisms, and in the balanced mode, gain and loss of introns might share common mechanistic features.

Figure 1.

Intron density in extant species and ancestral forms. Densities are measured in introns per 1000 nucleotides. (Blue bars) The observed values for genes from extant species, (yellow bars) the 95% confidence intervals for the densities in ancestral nodes, (internal separator) the optimal value. Species and lineage abbreviations: (Caeel) Caenorhabditis elegans, (Strpu) Strongylocentrotus purpuratus, (Cioin) Ciona intestinalis, (Danre) Danio rerio, (Galga) Gallus gallus, (Homsa) Homo sapiens, (Roden) Mus musculus and Rattus norvegicus combined, (Drome) Drosophila melanogaster, (Anoga) Anopheles gambiae, (Cryne) Cryptococcus neoformans, (Schpo) Schizosaccharomyces pombe, (Sacce) Saccharomyces cerevisiae, (Aspfu) Aspergillus fumigatus, (Neucr) Neurospora crassa, (Arath) Arabidopsis thaliana, (Orysa) Oryza sativa, (Thepa) Theileria parva, (Plafa) Plasmodium falciparum, (Dicdi) Dictyostelium discoideum, (AME) Ancestor of Multicellular Eukaryotes.

Figure 2.

Time dependence of the overall number of intron gain and loss events during eukaryotic evolution. (Green lines) Number of gain events, (red lines) number of loss events, (black lines) total number of events per species per 20 million yr (Myr). Events were counted in a 20-Myr window every 10 Myr. The results were smoothed using the moving average algorithm with a 31-time-points window. (Dashed lines) Highly conservative confidence intervals, obtained by taking the lowest and highest values in the 95% confidence interval of each lineage.

Figure 3.

Density of intron gain and loss events in extant species. (Green bars) 95% confidence interval of gains; (red bars) 95% confidence interval of losses; (central black line) the optimal value. Species abbreviations are as in Fig. 1. Density is measured as number of events per 1000 nucleotides.

Figure 4.

Distribution of intron gain and loss rates over the phylogenetic tree of eukaryotes. Node sizes are proportional to their (known or inferred) intron density, and the branches are color-coded: (green) predominant intron gain; (red) predominant intron loss; (blue) balanced gain and loss. The sole brown branch (Ascomycota) designates extensive (significantly greater than the mean over the tree) gains and losses. Species and lineage abbreviations are as in Fig. 1.

Figure 5.

Intron gain and loss rates of eukaryotic lineages. (Blue) Lineages exhibiting the balanced mode of evolution; (red) lineages with elevated loss rate; (green) lineages with elevated gain rate. The brown Ascomycota indicates the only lineage with both the gain rate and loss rate elevated. (Inset) An expanded view of the low-rate area that was obtained by excluding three lineages: Deuterostomia, Ascomycota, and S. cerevisiae. Selected lineages are labeled. Species and lineage abbreviations are as in Fig. 1.