The role of transposable elements in the evolution of non-mammalian vertebrates and invertebrates

Abstract

Background: Transposable elements (TEs) have played an important role in the diversification and enrichment of mammalian transcriptomes through various mechanisms such as exonization and intronization (the birth of new exons/introns from previously intronic/exonic sequences, respectively), and insertion into first and last exons. However, no extensive analysis has compared the effects of TEs on the transcriptomes of mammals, non-mammalian vertebrates and invertebrates.

Results: We analyzed the influence of TEs on the transcriptomes of five species, three invertebrates and two non-mammalian vertebrates. Compared to previously analyzed mammals, there were lower levels of TE introduction into introns, significantly lower numbers of exonizations originating from TEs and a lower percentage of TE insertion within the first and last exons. Although the transcriptomes of vertebrates exhibit significant levels of exonization of TEs, only anecdotal cases were found in invertebrates. In vertebrates, as in mammals, the exonized TEs are mostly alternatively spliced, indicating that selective pressure maintains the original mRNA product generated from such genes.

Conclusions: Exonization of TEs is widespread in mammals, less so in non-mammalian vertebrates, and very low in invertebrates. We assume that the exonization process depends on the length of introns. Vertebrates, unlike invertebrates, are characterized by long introns and short internal exons. Our results suggest that there is a direct link between the length of introns and exonization of TEs and that this process became more prevalent following the appearance of mammals.

Figure 1

Non-mammalian vertebrate and invertebrate genomes have lower levels of TEs than mammalian genomes. Evolutionary trees for chicken [30], zebrafish, sea squirt [62], Drosophila [63] and worm [63]. Percentages of TEs in each genome are shown on the right.

Figure 2

The fraction of introns containing TEs and their median lengths in non-mammalian and mammalian transcriptomes. (a) The fraction of TE-containing introns within five non-mammalian genomes compared to that of human (Homo sapiens) and mouse (Mus musculus) (for details see Materials and methods). (b) A graph of the median length of introns containing TEs compared to that of introns without TEs (marked in grey and black, respectively) in the different organisms. (c) Positive correlation between median intron length and the fraction of TEs containing introns. Intron lengths were taken from [17].

Figure 3

The effect of TEs on non-mammalian transcriptomes. (a) Summary of the number of exonized TEs in the different species. (i) Illustration of the exonization process, in which a TE (gray box) is inserted into an intron (line). Exonization of a TE may (ii) generate a cassette exon, (iii) create an alternative 5' splice site (Alt. 5' ss), (iv) create an alternative 3' splice site (Alt. 3' ss), or (v) be constitutively spliced (Const.). The table on the right shows the numbers of exonized TEs in each of the examined species. (b) Summary of the effect of TE insertions into the first or last exons. (i) Illustration of insertion of TEs (gray box) into an exon (white box). The insertion of the TEs may enlarge (ii) the first or (iii) the last exon.

Figure 4

Three cases of TE insertions into internal exons in D. melanogaster. Schematic representations of TE insertions into Drosophila internal exons. White boxes and lines represent exons and introns, respectively. The grey boxes show insertion of TEs into exons. The TE family is indicated beneath the gray box, along with the length of each inserted TE. Lengths of the introns and exons flanking the inserted exon are indicated. Genes with insertions are (a) cno, (b) CG14821 and (c) nej. CDS, coding sequence.

Figure 5

HE-1 SINE exonization in zebrafish. (a) Alignment of the HE1 SINE from D. rerio and the HE1 SINE from bullhead shark showing the different sections within the transposable element according to [43]. The letters y and r denote pyrimidine and purine, respectively. (b) Non-redundant distribution and orientation of exonized HE1 SINE sequences in which both the 5' and 3' splice sites are within the HE1 SINE sequence. The exonized HE1 SINE sequence regions are aligned against an HE1 SINE consensus element. Each line is a different EST showing exonizations and the box in the middle represents the HE1 element. The number of cases that select that site as a 5' splice site (73, 168, 44) or as a 3' splice site (11, 347) are shown. Exonizations in the sense and antisense orientations are shown above and below the schematic representation of the HE1.

Figure 6

Average lengths of first and last exons compared to the fraction of TEs inserted into exons. (a) The y-axis indicates average length of first exon in the six examined organisms (bars) and the percentage of base pairs that originated from TEs (line). (b) Similar analysis for last exons. Note that the y-axes are different in scale.