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BACKGROUND: Within eukaryotes, most horizontal transfer of genetic material involves mobile DNA sequences and such events are called horizontal transposable element transfer (HTT). Although thousands of HTT examples have been reported, the transfer mechanisms and their impacts on host genomes remain elusive.
RESULTS: In this work, we carefully annotated three Helitron families within several Xenopus frog genomes. One of the Helitron family, Heli1Xen1, is recurrently involved in capturing and shuffling Xenopus laevis genes required in early embryonic development. Remarkably, we found that Heli1Xen1 is seemingly expressed in X. laevis and has produced multiple genomic polymorphisms within the X. laevis population. To identify the origin of Heli1Xen1, we searched its consensus sequence against available genome assemblies. We found highly similar copies in the genomes of another 13 vertebrate species from divergent vertebrate lineages, including reptiles, ray-finned fishes and amphibians. Further phylogenetic analysis provides evidence showing that Heli1Xen1 invaded these lineages via HTT quite recently, around 0.58-10.74 million years ago.
CONCLUSIONS: The frequently Heli1Xen1-involved HTT events among reptiles, fishes and amphibians could provide insights into possible vectors for transfer, such as shared viruses across lineages. Furthermore, we propose that the Heli1Xen1 sequence could be an ideal candidate for studying the mechanism and genomic impact of Helitron transposition.
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Fig. 1. Helitron distribution in the genome of Xenopus frogs. A Phylogenetic tree of Xenopus Helitron transposases. The HeliNoto (from the fish Chionodraco hamatus) and Helitron- 9_OS (from the plant Oryza sativa) were chosen as positive controls because they are known autonomous Helitron2 and Helitron1 sequences from Repbase. Outgroup1 - 3 are three outgroup sequences. B Distribution of non-autonomous Helitrons in three Xenopus frogs. Frequency along the y-axis of Helitron insertions according to their length (x-axis, in bp). XT: X. tropicalis; XB: X. borealis; XL: X. laevis. The y-axis is square root adjusted. The star in red represents the WGD event that happened ~ 34 mya
Fig. 2. Landscape of captured gene fragments within Helitron insertions. A Sequence logos of terminal sequences of LTS and RTS for nonautonomous Heli1Xen1 involving in gene capture events. Red arrows on top of the graph indicate the pattern of Helitron insertion sites. B Nucleotide identity between the donor gene and captured fragments. C Length of captured CDS fragments by Helitron sequences. D Relative start position of captured fragments within the donor gene, zero corresponds to the 5’ end of the CDS and 0.8 to the 3’ end. E Number of Helitron insertions that contain the gene fragments
Fig. 3. Genomic landscape of the X. laevis Heli1Xen1 locus. This locus is annotated as gene LOC108706566 (the blue part indicates the 5’ UTR region, and the yellow part indicates the CDS region) by the NCBI annotation pipeline and as a Helitron insertion by HELIANO. The Chip-seq profile of animal cap NF18 shows significant foxn4 and myb Chip-seq peaks (TPM) at the 5’ end of this locus. The RNA-seq reads collected from blastema cells in either non-proliferating or proliferating status are uniquely mapped on this locus [22]
Fig. 4. Heli1Xen1 polymorphism in X. laevis genomes. A Heli1Xen1 polymorphism distribution across chromosomes of X. laevis. The blue bar represents the density of Heli1Xen1 insertions every 100 kbp window in the X. laevis reference genome. Dots in purple represent the insertion of Heli1Xen1 in the outbred genomes. Green triangles represent the absence of Heli1Xen1 in the outbred genomes. B The histogram shows the frequency of detected Heli1Xen1 polymorphisms according to their length expressed in bp
Fig. 5. Heli1Xen1 sequences in vertebrates. The heatmap (left) shows the pairwise identity of Heli1Xen1 RepHel consensus sequences from the different vertebrates where it was found. Each cell indicates the percentage of nucleotide identity. The bar plot (right) shows the number of autonomous and non-autonomous Heli1Xen1 insertions in each vertebrate genome. The phylograms on the left and the top of the heatmap are based on Time Tree database
Fig. 6. Classification of homologous HeliXen1 sequences across vertebrates. A Phylogenetic relationships of HeliXen1 RepHel sequences from different vertebrates. Heli1Xen1-a and Heli1Xen1-b are highlighted in different colours. Heli1Xen2 and Helitron- 9_OS are used as the outgroup. B-C Plots show the PhastCons score across Heli1Xen1-a (B) and Heli1Xen1-b (C) consensus sequences from X. laevis and Polypterus senegalus (a ray-finned fish), respectively. The position of RepHel ORF is highlighted in red
Fig. 7. Histogram of the Kimura substitution distribution between orthologous genes of X. laevis and other vertebrates. The red dotted line indicates the Kimura substitutions between Heli1Xen1 from X. laevis and each vertebrate genome
Fig. 8. Length distribution of Heli1Xen1 insertions in different species genomes. Non-autonomous insertions are shown in red, and autonomous insertions in blue. Species are ordered based on their phylogeny relationship. The X-axis represents the insertions' length (bp), and the Y-axis represents the number of insertions log10-adjusted. The dotted line represents the peaks of size distribution
Supplementary Figure S1. Analysis of tandem arrays in HLEs. (A) Dotplot of the
longest locus containing a tandem duplication of an Heli1Xen1 non-autonomous
element. Arrows correspond to the duplicated Heli1Xen1 insertion. (B) Dotplot of the
longest locus containing a tandem duplication of an Heli2Xen non-autonomous
element. Long arrows correspond to the duplicated Heli2Xen insertion, small
arrowheads correspond to the minisatellite array. (C) Top: Dotplot comparison of the
Heli2Xen autonomous element (horizontal) and of its minisatellite motif of 166 bp
(vertical). Bottom: domain architecture of the Heli2Xen sequence obtained from the
NCBI CDD server. Note the domains corresponding to the RepHel transposase.
Dotplot were made using Yass (https://bioinfo.cristal.univ-lille.fr/yass/index.php).
Supplementary Figure S . Two Heli1Xen1 insertions containing the complete CDS
sequence of the transmembrane protein 111 (tmem111.S) gene. The highlighted red
region refers to the tmem111.S transcript sequence.
Supplementary Figure S3. (A) Autonomous Heli1Xen1 insertion in X. laevis genome
and its transposase sequence. The complete ORF is highlighted in orange; The start
codon is highlighted in red, and the stop c odon in purple. (B) Scheme shows the
conserved transposase domain of the ORF region of Heli1Xen1 insertion
Xenopus_laevis_4: ‘Helitron_like_N’ represents the approximate region of Rep
domains and ‘DEAD-like_helicase_N_superfamily’ represents region of Helicase
domain. Image obtained from the Conserved Domain Database (CDD) search tool (Lu
et al. 2020).
Supplementary Figure S3. (A) Autonomous Heli1Xen1 insertion in X. laevis genome
and its transposase sequence. The complete ORF is highlighted in orange; The start
codon is highlighted in red, and the stop c odon in purple. (B) Scheme shows the
conserved transposase domain of the ORF region of Heli1Xen1 insertion
Xenopus_laevis_4: ‘Helitron_like_N’ represents the approximate region of Rep
domains and ‘DEAD-like_helicase_N_superfamily’ represents region of Helicase
domain. Image obtained from the Conserved Domain Database (CDD) search tool (Lu
et al. 2020).
Supplementary Figure S4. IGV plots indicate examples showing the Heli1Xen1
absence in outbred frogs and presence in J-strain (inbred). The reads for J-strain are
the same reads for assembly of X. laevis reference genome.
Supplementary Figure S4. IGV plots indicate examples showing the Heli1Xen1
absence in outbred frogs and presence in J-strain (inbred). The reads for J-strain are
the same reads for assembly of X. laevis reference genome.
Supplementary Figure S5. Terminal sequences of Heli1Xen1 in each species. LTS:
Left terminal sequence; RTS: Right terminal sequence.
