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Comparative Study
, 8 (10), R223

Comparative Genomic Analysis of Fungal Genomes Reveals Intron-Rich Ancestors

Affiliations
Comparative Study

Comparative Genomic Analysis of Fungal Genomes Reveals Intron-Rich Ancestors

Jason E Stajich et al. Genome Biol.

Abstract

Background: Eukaryotic protein-coding genes are interrupted by spliceosomal introns, which are removed from transcripts before protein translation. Many facets of spliceosomal intron evolution, including age, mechanisms of origins, the role of natural selection, and the causes of the vast differences in intron number between eukaryotic species, remain debated. Genome sequencing and comparative analysis has made possible whole genome analysis of intron evolution to address these questions.

Results: We analyzed intron positions in 1,161 sets of orthologous genes across 25 eukaryotic species. We find strong support for an intron-rich fungus-animal ancestor, with more than four introns per kilobase, comparable to the highest known modern intron densities. Indeed, the fungus-animal ancestor is estimated to have had more introns than any of the extant fungi in this study. Thus, subsequent fungal evolution has been characterized by widespread and recurrent intron loss occurring in all fungal clades. These results reconcile three previously proposed methods for estimation of ancestral intron number, which previously gave very different estimates of ancestral intron number for eight eukaryotic species, as well as a fourth more recent method. We do not find a clear inverse correspondence between rates of intron loss and gain, contrary to the predictions of selection-based proposals for interspecific differences in intron number.

Conclusion: Our results underscore the high intron density of eukaryotic ancestors and the widespread importance of intron loss through eukaryotic evolution.

Figures

Figure 1
Figure 1
This figure depicts a phylogenetic tree of the species used for this analysis. The tree is based on Bayesian phylogenetic reconstruction of 30 aligned orthologous proteins from the 25 species. The numbers after the species names list the total number of introns present in the CORs for each species. U. maydis is colored purple to indicate it has a different intron pattern than the rest of the basidiomycete fungi sampled. Numbers in boxes are node numbers that are used in Tables seen Additional data files 4 and 5.
Figure 2
Figure 2
Intron length versus average number of introns per kilobase. Colored boxes indicate the fungal clade as shown in Figure 1: red, Hemiascomycota; yellow, Archiascomycota; green, Euascomycota; orange, Zygomycota; blue, Basidiomycota; purple, basidiomycete U. maydis. Bars indicating standard deviation in intron length are drawn but only visible for the intron-poor species. CDS, coding sequence.
Figure 3
Figure 3
Pattern of intron sharing of fungal species. Fractions of intron positions that are shared with animal or plant (A+P), plant, animal, with another fungal clade (Euascomycota, Hemiascomycota, or Basidiomycota), or specific to the species or clade.
Figure 4
Figure 4
Fraction of shared plant-animal intron positions in each fungal species. Among the 501 intron positions that are shared between A. thaliana and a vertebrate (and thus likely present in the fungus-animal ancestor), the fraction that is shared with each fungal species is given. Color coding is lavender: introns found only within the clade or a single species, maroon: introns shared only with other fungi,, pink: introns shared with animals, green: introns shared with plants (A. thaliana), brown: introns shared with animals or plants.
Figure 5
Figure 5
Estimated number of introns per kilobase in CORs through fungal history using the EREM method. Numbers in ovals give estimated ancestral values normalized by the total number of aligned bases in the CORs (4.15 Mb). Numbers in black boxes represent the node number references in the tables in Additional data files 4 and 5. Blue branches indicate two or more estimated losses for each estimated gain; red > 1.5 gains per loss. (a) Summarized fungal tree. Triangles indicate clades, with values for the clade ancestor indicated. (b) Introns per kilobase through Euascomycota history, the clade indicated by the grey box in (a).
Figure 6
Figure 6
Performance of Csűrös, RG, Dollo parsimony, and EREM methods for the four-taxa case under intron loss rate variation with loss rates given by a standard gamma distribution with indicated alpha value, in which 30% or 70% of introns are lost along each external branch. The actual number of simulated ancestral intron numbers is 1,000; thus, both Csűrös and Dollo methods underestimate ancestral density under all cases. The relevant phylogeny is given in Additional file 2.

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