Bursts and horizontal evolution of DNA transposons in the speciation of pseudotetraploid salmonids

Abstract

Background: Several genome duplications have occurred in the evolutionary history of teleost fish. In returning to a stable diploid state, the polyploid genome reorganized, and large portions are lost, while the fish lines evolved to numerous species. Large scale transposon movement has been postulated to play an important role in the genome reorganization process. We analyzed the DNA sequence of several large loci in Salmo salar and other species for the presence of DNA transposon families.

Results: We have identified bursts of activity of 14 families of DNA transposons (12 Tc1-like and 2 piggyBac-like families, including 11 novel ones) in genome sequences of Salmo salar. Several of these families have similar sequences in a number of closely and distantly related fish, lamprey, and frog species as well as in the parasite Schistosoma japonicum. Analysis of sequence similarities between copies within the families of these bursts demonstrates several waves of transposition activities coinciding with salmonid species divergence. Tc1-like families show a master gene-like copying process, illustrated by extensive but short burst of copying activity, while the piggyBac-like families show a more random copying pattern. Recent families may include copies with an open reading frame for an active transposase enzyme.

Conclusion: We have identified defined bursts of transposon activity that make use of master-slave and random mechanisms. The bursts occur well after hypothesized polyploidy events and coincide with speciation events. Parasite-mediated lateral transfer of transposons are implicated.

Figure 1

Phylogenetic tree of DNA transposon sequences in Salmo salar and various other species. A) Tc1-like DNA transposons; B) piggyBac-like DNA transposons. Sequence alignments were performed with ClustalW and phylogenetic trees generated with MEGA3.1 using the Unweighted Pair Group Method with Arithmetic Mean (UPGMA), pairwise deletion, and a p-distance model. Sequences used in the tree are at least 1000 bp, but EST sequences from Schistosoma japonicum are between 500 and 700 bp long. DTSsa3 is not included in the tree as only fragments of a few hundred base pairs were recovered that conform to the amino acid motifs required for a Tc1-like transposon. DTSsa5 has two copies that are closely related due to a recent duplication event. Shown below are the color markers for the species. No marker in the tree indicates Salmo salar. All others are: Acanthophthalmus kuhli; Astatotilapia burtoni; Carassius auratus; Cyprinus carpio; Danio rerio; Deltistes luxatus; Esox lucius; Gasterosteus aculeatus; Ictalurus punctatus; Oncorhynchus kisutch; Oncorhynchus mykiss; Oncorhynchus tsawytscha; Oryzias latipes; Petromyzon marinus; Polypterus bichir; Rana pipiens; Salvelinus fontinalis; Schistosoma japonicum; Tanichthys albonubus; Xenopus tropicalis; Xenopus laevis.

Figure 2

Terminal repeat structure. Inverted Terminal Repeat of examples of recovered members of the DTSsa1 (upper sequence) and SSTN1 (lower sequence) families. The TA insertion site is shown at the start of the sequences, followed by the canonical CAGT. The two direct repeated sequences at the two ends of an ITR are in bold and underlined.

Figure 3

Bursts of DNA transposon activity. Horizontal bars represent the duration of bursts of Tc1-like DNA transposon in Salmo salar, based on earliest and latest branching. The shaded areas indicate the approximate timing of the genome duplication event (left) and further speciation events [4] (right).