Tittarelli E et al. (2025), Transposable element dynamics in Xenopus laevis...

XB-ART-61344

Mob DNA 2025 Apr 09;161:17. doi: 10.1186/s13100-025-00350-3.

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Transposable element dynamics in Xenopus laevis embryogenesis: a tale of two coexisting subgenomes.

Tittarelli E , Carotti E , Carducci F , Barucca M , Canapa A , Biscotti MA .

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The African clawed frog Xenopus laevis has an allotetraploid genome consisting of two subgenomes referred as L relating to the Long chromosomes and S relating to the Short chromosomes. While the L subgenome presents conserved synteny with X. tropicalis chromosomes, the S subgenome has undergone rearrangements and deletions leading to differences in gene and transposable element (TE) content between the two subgenomes. The asymmetry in the evolution of the two subgenomes is also detectable in gene expression levels and TE mobility. TEs, also known as "jumping genes", are mobile genetic elements having a key role in genome evolution and gene regulation. However, due to their potential deleterious effects, TEs are controlled by host defense mechanisms such as the nucleosome remodeling and deacetylase (NuRD) complex and the Argonaute proteins that mainly modify the heterochromatin environment. In embryogenesis, TEs can escape the silencing mechanisms during the maternal-to-zygotic transition when a transcriptionally permissive environment is created. Moreover, further evidence highlighted that the reactivation of TEs during early developmental stages is not the result of this genome-wide reorganization of chromatin but it is class and stage-specific, suggesting a precise regulation. In line with these premises, we explored the impact of TE transcriptional contribution in six developmental stages of X. laevis. Overall, the expression pattern referred to the entire set of transcribed TEs was constant across the six developmental stages and in line with their abundance in the genome. However, focusing on subgenome-specific TEs, our analyses revealed a distinctive transcriptional pattern dominated by LTR retroelements in the L subgenome and LINE retroelements in the S subgenome attributable to young copies. Interestingly, genes encoding proteins involved in maintaining the repressive chromatin environment were active in both subgenomes highlighting that TE controlling systems were active in X. laevis embryogenesis and evolved symmetrically.

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Species referenced: Xenopus laevis
Genes referenced: ago1 ago2 ago3 ago4 cbx1 cbx3 cbx5 chd3 chd4 dnmt1 dnmt3a gatad2a gatad2b hdac1 hdac2 mbd2 mbd3 mta1 mta2 rbbp4 rbbp7 setdb1 trim28
GO keywords: embryo development

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	Fig. 1. Repeat contribution and Kimura landscapes in the Xenopus laevis genome and subgenomes. A. On the left, the repeat landscape plot obtained by Kimura distance-based copy divergence analyses of TEs in X. laevis total genome. On the right, aerogram with TE type percentage of genome composition. B. Aerograms with TE type percentage of each subgenome compositions and repeat landscape plots obtained by Kimura distance-based copy divergence analyses of TEs in the X. laevis L and S subgenomes, respectively. C. Aerograms with subgenome-specific TE type percentage and repeat landscape plots obtained by Kimura distance-based copy divergence analyses of subgenome-specific TEs, respectively. In all panels, “unclear” means TEs that are not specifically classified as DNA transposons, LINE, SINE, and LTR retrotransposons, “non-LTR” retrotransposons are referred to retrotransposons that are not specifically classified as LINE or SINE retrotransposons, and “Retro” is referred to retrotransposons that are not specifically classified as LINE, SINE, LTR or non-LTR retrotransposons
	Fig. 2. Transcriptional contribution of TEs in X. laevis early development and Kimura landscapes. In the upper side, the transcriptional contribution of TEs as percentage of mapped reads was reported in six developmental stages. In the lower side, the repeat landscape plots obtained by Kimura distance-based copy divergence analyses of transcribed TEs were reported. “Unclear” means TEs that are not specifically classified as DNA transposons, LINE, SINE, and LTR retrotransposons, “non-LTR” retrotransposons are referred to retrotransposons that are not specifically classified as LINE or SINE retrotransposons, and “Retro” is referred to retrotransposons that are not specifically classified as LINE, SINE, LTR or non-LTR retrotransposons
	Fig. 3. Volcano plot of differentially expressed TEs (DETEs) during developmental stages of X. laevis. From left to right, each graph reports the results of comparisons between the considered developmental stages (Blastula vs. Zygote, Gastrula vs. Blastula, Neurula vs. Gastrula, Tailbud vs. Gastrula, and Early tailbud vs. Tailbud). The blue dashed lines indicate the significant thresholds for Log2 Fold Change >\|2\|, while the red dashed the statistically significant threshold (-Log10 (p-adj) = 0.05). Each dot represents a single DETE and the color indicates the TE typology (DNA transposons in blue, LINE retroelements in orange, LTR retroelements in grey, SINE retroelements in yellow, Unknown, referred to TEs that are not classified as the previous typologies, in green)
	Fig. 4. Cumulative transcriptional activity of subgenome-specific TEs. On the left, cumulative transcriptional levels of L subgenome-specific TEs were reported; On the right, cumulative transcriptional levels of S subgenome-specific TEs were reported. “Unclear” means TEs that are not specifically classified as DNA transposons, LINE, SINE, and LTR retrotransposons, “non-LTR” retrotransposons are referred to retrotransposons that are not specifically classified as LINE or SINE retrotransposons, and “Retro” is referred to retrotransposons that are not specifically classified as LINE, SINE, LTR or non-LTR retrotransposons
	Fig. 5. Volcano plot of subgenome-specific differentially expressed TEs (DETEs) during developmental stages of X. laevis. From left to right, each graph reports the results of comparisons between the considered developmental stages (Blastula vs. Zygote, Gastrula vs. Blastula, Neurula vs. Gastrula, Tailbud vs. Gastrula, and Early tailbud vs. Tailbud). The blue dashed lines indicate the significant thresholds for Log2 Fold Change >\|2\|, while the red dashed the statistically significant threshold (-Log10 (p-adj) = 0.05). DETEs common to L and S subgenomes are reported in light grey; L subgenomes-specific DETEs are colored in purple; S subgenome-specific DETEs are colored in turquoise. The colored dots without label are referred to “unclear”, TEs that are not specifically classified as DNA transposons, LINE, SINE, and LTR retrotransposons
	Fig. 6. Kimura landscapes of transcribed subgenome-specific TEs during X. laevis development. Repeat landscape plots obtained by Kimura distance-based copy divergence analyses of L and S subgenome-specific TEs transcribed in six developmental stages. “Unclear” means TEs that are not specifically classified as DNA transposons, LINE, SINE, and LTR retrotransposons, “non-LTR” retrotransposons are referred to retrotransposons that are not specifically classified as LINE or SINE retrotransposons, and “Retro” is referred to retrotransposons that are not specifically classified as LINE, SINE, LTR or non-LTR retrotransposons
	Fig. 7. Transcriptional activity of genes involved in TE silencing mechanisms during X. laevis early development in the L subgenome. A. Expression values of genes encoding KRAB-ZFPs. B. Expression values of genes encoding proteins involved in the formation of the heterochromatin and NuRD complex. C. Expression values of genes encoding proteins of Argonaute subfamily
	Fig. 8. Transcriptional activity of genes involved in TE silencing mechanisms during X. laevis early development in the S subgenome. A. Expression values of genes encoding KRAB-ZFPs. B. Expression values of genes encoding proteins involved in the formation of the heterochromatin and NuRD complex. C. Expression values of genes encoding proteins of Argonaute subfamily. The broken line along the Y axis indicates the range of values from 300 to 700 TPM