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Front Genet
2022 Jan 01;13:766424. doi: 10.3389/fgene.2022.766424.
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Activation of DNA Transposons and Evolution of piRNA Genes Through Interspecific Hybridization in Xenopus Frogs.
Suda K
,
Hayashi SR
,
Takamatsu N
,
Ito M
.
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Interspecific hybridization between two closely related species sometimes resulted in a new species with allotetraploid genomes. Many clawed frog species belonging to the Xenopus genus have diverged from the allotetraploid ancestor created by the hybridization of two closely related species with the predicted L and S genomes. There are species-specific repeated sequences including transposable elements in each genome of organisms that reproduce sexually. To understand what happened on and after the hybridization of the two distinct systems consisting of repeated sequences and their corresponding piRNAs, we isolated small RNAs from ovaries and testes of three Xenopus species consisting of allotetraploid X. laevis and X. borealis and diploid X. tropicalis as controls. After a comprehensive sequencing and selection of piRNAs, comparison of their sequences showed that most piRNA sequences were different between the ovaries and testes in all three species. We compared piRNA and genome sequences and specified gene clusters for piRNA expression in each genome. The synteny and homology analyses showed many distinct piRNA clusters among the three species and even between the two L and/or S subgenomes, indicating that most clusters of the two allotetraploid species changed after hybridization. Moreover, evolutionary analysis showed that DNA transposons including Kolobok superfamily might get activated just after hybridization and then gradually inactivated. These findings suggest that some DNA transposons and their piRNAs might greatly influence allotetraploid genome evolution after hybridization.
Figure 1. Strategy for genome-wide analysis of piRNAs and repeat sequences including TEs in a diploid and two allotetraploid Xenopus frog species.
Figure 2. Sequence characterization of ovarian and testicular piRNAs in the three Xenopus species, X. tropicalis, X. laevis, and X. borealis. Distributions of 5′-overlap lengths (left) and 1 U/10 A bias (right) on piRNA molecules transcribed in ovaries (A) and testes (B). The amounts of piRNAs were normalized by 107/mapped piRNA counts in length distribution. Numbers of sequence types of piRNAs transcribed in testes and ovaries are shown in Venn diagrams (C).
Figure 3. Landscapes of DNA transposons and retrotransposons in the three Xenopus species. The substitution ratios of DNA transposons (blue) and retrotransposons (red) in X. tropicalis (A), X. laevis L and S (B), and X. borealis L and S (C) are shown on the horizontal axis. Proportion (%) of the transposons to each genome DNA are shown on the vertical axis. The numbers 34 and 17 indicate speciation and hybridization time (mya) of the predicted L and S species, which correspond to the substitution ratios, 0.10 and 0.05, respectively.
Figure 4. Landscapes of six major superfamilies of DNA transposons in the three Xenopus species. The substitution ratio of each superfamily in X. tropicalis (A), X. laevis L and S (B), and X. borealis L and S (C) are shown on the horizontal axis. Proportion (%) of the transposons to each genome DNA are shown on the vertical axis.
Fig. S1. Distributions of lengths of plus (red) and minus (blue) stranded piRNA molecules transcribed in ovaries and testes.
Fig. S2. Numbers of testicular and ovarian piRNAs from three Xenopus frog species in venn diagrams. The intersection of the diagram corresponds to the identical sequences between the two.
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Fig. S3. Distributions of 5’-overlap lengths and 1U/10A bias on four types of piRNA molecules from ovaries and testes in three Xenopus species. Four types include DNA transposon-derived piRNAs (A and B), retrotransposon-derived piRNAs (C and D), exon-derived piRNAs (E and F), and intron-derived piRNAs (G and H). A, C, E, and G, or B, D, F, and H indicate ovarian or testicular piRNAs, respectively.
Fig. S4. Positions of piRNA clusters transcribed in ovaries and testes on each chromosome of X. tropicalis (Xt), X. laevis (Xl) and X. borealis (Xb). Red and blue lines indicate the positions of the clusters from ovaries and testes, respectively, on each chromosome.
Fig. S5. Percentage of DNA components to (sub)genomes and piRNA clusters from ovaries and testes in the three Xenopus species.
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