Transduplication resulted in the incorporation of two protein-coding sequences into the Turmoil-1 transposable element of C. elegans
© Sela et al; licensee BioMed Central Ltd. 2008
Received: 03 October 2008
Accepted: 08 October 2008
Published: 08 October 2008
Transposable elements may acquire unrelated gene fragments into their sequences in a process called transduplication. Transduplication of protein-coding genes is common in plants, but is unknown of in animals. Here, we report that the Turmoil-1 transposable element in C. elegans has incorporated two protein-coding sequences into its inverted terminal repeat (ITR) sequences. The ITRs of Turmoil-1 contain a conserved RNA recognition motif (RRM) that originated from the rsp-2 gene and a fragment from the protein-coding region of the cpg-3 gene. We further report that an open reading frame specific to C. elegans may have been created as a result of a Turmoil-1 insertion. Mutations at the 5' splice site of this open reading frame may have reactivated the transduplicated RRM motif.
This article was reviewed by Dan Graur and William Martin. For the full reviews, please go to the Reviewers' Reports section.
The possible contribution of transposable elements to the proteome has been discussed in several publications [1–7] and has provoked much debate . Many mechanisms are known to increase the protein-domain repertoire, e.g., domain duplication, substitution mutations, insertions, deletions, and domain rearrangements . In metazoans, a transposable element may result in transduction, in which a DNA segment downstream of transposable elements is mobilized as part of an aberrant transposition. This may result in gene duplication or exon shuffling, subsequently enriching the protein repertoire [10–13]. However, in the process of transduction, the transposable element does not acquire gene fragments as part of its sequence.
In plants, on the other hand, thousands of transposable elements contain duplicated gene fragments, captured in a process termed transduplication. Transduplication is a potentially rich source of novel coding sequences within rice and Arabidopsis thaliana [14–16]. Recently, transduplications of small nucleolar (sno) RNA by retroposon-like non-LTR transposable elements were found in the C. elegans  and platypus genomes .
The Harbinger superfamily of "cut-and-paste" DNA transposons was discovered through in silico studies . This superfamily is characterized by Harbinger-specific transposases that are distantly related to the transposases encoded by the IS5-like group of bacterial transposons, such as IS5, IS112, and ISL2. Harbinger transposons are not as widespread as the eukaryotic hAT and mariner/Tc1 transposons; they are found in plants and nematodes [19–23] but not in mammals. Usually, Harbinger transposons are flanked by 3-bp target site duplications and 25- to 50-bp inverted terminal repeats (ITRs).
Turmoil-1 elements within the C. elegans genome
Containing RRM domain (***)
Containing cpg-3 fragment
Length of the element (****)
A comparative analysis of the rsp-2 gene and the 205-bp region of the gene found in the ITR sequence, revealed that the Turmoil-1 sequence has accumulated several point mutations within the 5' splice site that make it non-functional, whereas the 3' splice site of the intron remains intact (the mutations in the 5' splice site region are marked in red in Figure 1B). Since the RRM domain within the Turmoil-1 DNA transposon is not under purifying selection to maintain the reading frame or the functionality of the splice sites, these mutations are not unexpected.
Within the same ITR domain of Turmoil-1, and very close to the site of insertion of the RRM domain of rsp-2 gene, there is evidence of another "DNA kidnapping" event. A 131-bp fragment from the coding region of C. elegans gene cpg-3, which is unique to nematodes, was inserted into the ITR (Figure 1C). No sequences homologous to Turmoil-1 flank the cpg-3 gene. Thus, similar to the rsp-2 case, a gene fragment from the cpg-3 most likely was acquired by Turmoil-1, and not vice-versa. As the gene fragments are present on both sides of the ITR, capture may have occurred through non-homologous recombination.
Our analysis indicates that Turmoil-1 of C. elegans has captured two unrelated coding sequences within its ITRs at proximate locations. The presence of a transduplication "hotspot" in this region may be tentatively inferred. This analysis reveals a transduplication of protein-coding regions in C. elegans and strengthens the hypothesis that protein domains may be mobilized by transposable elements.
Reviewer's report 1: Dan Graur, Department of Biology & Biochemistry University of Houston, Texas, USA
A very straightforward report – I have no other comments.
Reviewer's report 2: William Martin, Institut fuer Botanik III, Heinrich-Heine Universitaet Duesseldorf, Germany
This is an interesting and straightforward paper reporting the presence of transduplication in Caenorhabditis. The report of transduplication in animals would appear to be novel and certainly of sufficient interest to warrant publication. It might be the seed of a larger transduplication avalanche in animals, we'll see. I think the paper is fine for publication with the exception of "open read [ing] frame" in the abstract.
Thanks for your comment – the typo was corrected.
RNA Recognition motif
inverted terminal repeat
open reading frame.
We thank Prof. Jerzy Jurka for critical reading of the manuscript. This work was supported by the Israeli Ministry of Science and Technology (MOST) and by grants from the Israel Science Foundation (1449/04 and 40/05), MOP Germany-Israel, GIF, ICA through the Ber-Lehmsdorf Memorial Fund, and DIP and EURASNET. AS is a fellow of the Complexity Science Scholarship program and is supported by a fellowship from the Israeli Ministry of Science.
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