Patterns of exon-intron architecture variation of genes in eukaryotic genomes

Abstract

Background: The origin and importance of exon-intron architecture comprises one of the remaining mysteries of gene evolution. Several studies have investigated the variations of intron length, GC content, ordinal position in a gene and divergence. However, there is little study about the structural variation of exons and introns.

Results: We investigated the length, GC content, ordinal position and divergence in both exons and introns of 13 eukaryotic genomes, representing plant and animal. Our analyses revealed that three basic patterns of exon-intron variation were present in nearly all analyzed genomes (P < 0.001 in most cases): an ordinal reduction of length and divergence in both exon and intron, a co-variation between exon and its flanking introns in their length, GC content and divergence, and a decrease of average exon (or intron) length, GC content and divergence as the total exon numbers of a gene increased. In addition, we observed that the shorter introns had either low or high GC content, and the GC content of long introns was intermediate.

Conclusion: Although the factors contributing to these patterns have not been identified, our results provide three important clues: common factor(s) exist and may shape both exons and introns; the ordinal reduction patterns may reflect a time-orderly evolution; and the larger first and last exons may be splicing-required. These clues provide a framework for elucidating mechanisms involved in the organization of eukaryotic genomes and particularly in building exon-intron structures.

Figure 1

Variation patterns of introns' length, as a function of GC content. Each dot contains 1000 introns (A-D). The species in A-C were grouped based on ranges of intron lengths, e.g., up to 16000 bp for mammals. L1, L2, H1, H2 and H3 in D represent five GC-isochore families in human genome [22] which are different in GC content (0~0.37, 0.37~0.41, 0.41~0.46, 0.46~0.53, 0.53~1, respectively). Genes that cover two or more family regions were excluded in D. The x-axis scale in A – D is based on the actual GC content in different genomes.

Figure 2

Variation patterns of intron (A) or exon length (B), as a function of its ordinal number. Only introns or exons with ordinal numbers ≤ 40 were shown in the figures; each dot contains > 1000 samples.

Figure 3

Variation patterns of exon GC content, as a function of flanking intron GC content (A~D), and exon length, as a function of flanking logarithmical intron length (E~H). Each dot contains 1000 introns and 1000 exons (1000 left exons flanking the corresponding introns). Introns used in E~H are > 100 bp.

Figure 4

Correlation between nucleotide divergence (or exon's Ka) and ordinal position of introns (A & B) or of exons (C & D) and between intron and flanking exon divergence (or Ka) (E & F). The left panel shows the results from the comparison between human and chimpanzee, and the right panel shows the comparison between two rice lines.

Figure 5

Correlations between the length and intron (A) or exon (B) count, between GC content and intron (C) or exon (D) count and between the nucleotide divergence and intron (E) or exon (F) count. The number (count) in the horizontal axis stands for the 1, 2-,..., 9 and 10-intron (or -exon) genes.