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. 2011:3:1-14.
doi: 10.1093/gbe/evq080. Epub 2010 Dec 2.

The evolution and diversity of DNA transposons in the genome of the Lizard Anolis carolinensis

Peter A Novick  1 , Jeremy D Smith, Mark Floumanhaft, David A Ray, Stéphane Boissinot
Affiliations

The evolution and diversity of DNA transposons in the genome of the Lizard Anolis carolinensis

Peter A Novick et al. Genome Biol Evol. 2011.

Abstract

DNA transposons have considerably affected the size and structure of eukaryotic genomes and have been an important source of evolutionary novelties. In vertebrates, DNA transposons are discontinuously distributed due to the frequent extinction and recolonization of these genomes by active elements. We performed a detailed analysis of the DNA transposons in the genome of the lizard Anolis carolinensis, the first non-avian reptile to have its genome sequenced. Elements belonging to six of the previously recognized superfamilies of elements (hAT, Tc1/Mariner, Helitron, PIF/Harbinger, Polinton/Maverick, and Chapaev) were identified. However, only four (hAT, Tc1/Mariner, Helitron, and Chapaev) of these superfamilies have successfully amplified in the anole genome, producing 67 distinct families. The majority (57/67) are nonautonomous and demonstrate an extraordinary diversity of structure, resulting from frequent interelement recombination and incorporation of extraneous DNA sequences. The age distribution of transposon families differs among superfamilies and reveals different dynamics of amplification. Chapaev is the only superfamily to be extinct and is represented only by old copies. The hAT, Tc1/Mariner, and Helitron superfamilies show different pattern of amplification, yet they are predominantly represented by young families, whereas divergent families are exceedingly rare. Although it is likely that some elements, in particular long ones, are subjected to purifying selection and do not reach fixation, the majority of families are neutral and accumulate in the anole genome in large numbers. We propose that the scarcity of old copies in the anole genome results from the rapid decay of elements, caused by a high rate of DNA loss.

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Figures

F<sc>IG</sc>. 1.—
FIG. 1.—
Phylogenetic position of Anolis hATs relative to previously described hAT families. The tree is based on an amino acid alignment of the transposase domain. It was inferred using the neighbor joining method, and the robustness of the nodes was assessed by bootstrap (1,000 runs). Bootstrap values <75% have been removed.
F<sc>IG</sc>. 2.—
FIG. 2.—
Neighbor joining phylogeny of autonomous hobo_AC elements based on 3 kb of the transposase domain. The boxed sequences indicate elements that are complete in the genome assembly we used. The presence of nested TE in complete hobo_AC elements was determined by running Repeatmasker with a library of repetitive sequences found in the anole genome. Seven different patterns of nested elements were recovered and are schematically presented on the right of each sequence (structure 3 corresponds to elements 93, 13, 10, and 253). Though all 45 elements are very similar to each other, they differ in their length and structure. The arrows on the right indicate the recombination of elements 3 and 4 resulting in element 1.
F<sc>IG</sc>. 3.—
FIG. 3.—
(A) 5′ and 3′ termini of consensus sequences of autonomous and nonautonomous hobo_AC families. The TIRs are boxed. Although these 16 families have similar 5′ and 3′ ends, they differ considerably in their central region due to a large number of indels and transposon insertions. Thus, the central region is unique and specific of a given family; (B) Neighbor joining trees based on 150 bp of the 5′ region (left) and 300 bp of the 3′ region (right) of nonautonomous hobo_AC elements. Bootstrap values less than 75% have been removed. At least three elements from each family are included. Boxes around elements reveal the group swap of hobo-N14_AC (blue) and hobo-N15_AC (red) in group A (light red) and group B (light blue) due to interelements recombination.
F<sc>IG</sc>. 4.—
FIG. 4.—
Diagram depicting the evolution of the 15 nonautonomous hobo families (see text for explanation).
F<sc>IG</sc>. 5.—
FIG. 5.—
Divergence plot of hAT (red), Tc1/Mariner (orange), Helitron (yellow), and Chapaev (green) families found in the genome of the lizard. Values were calculated using Kimura's 2-parameter method in Mega 4.0. Autonomous families are emphasized with darker bars.
F<sc>IG</sc>. 6.—
FIG. 6.—
Phylogenetic position of the only autonomous Tc1/Mariner family in anole relative to previously described Mariner families. The tree is based on an amino acid alignment of the transposase domain. It was built using the neighbor joining method and the robustness of the nodes was assessed by bootstrap (1,000 runs). Bootstrap values <65% have been removed.
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