Suda K et al. (2024), Correlation Between Subgenome-biased DNA Loss a...

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Genome Biol Evol 2024 Sep 03;169:. doi: 10.1093/gbe/evae179.

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Correlation Between Subgenome-biased DNA Loss and DNA Transposon Activation Following Hybridization in the Allotetraploid Xenopus Frogs.

Suda K , Suzuki T , Hayashi S , Okuyama H , Tsukamoto D , Matsuo T , Tamura K , Ito M .

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In certain tetraploid species resulting from interspecific hybridization, one parent's subgenome is known to selectively undergo DNA loss. The molecular mechanisms behind this remain unclear. In our study, we compared the genomes of a standard diploid species with two allotetraploid species from the Xenopus genus, both possessing L (longer) and S (shorter) homoeologous subgenomes. We observed substantial gene losses and intergenic DNA deletions in both the S and L subgenomes of the tetraploid species. Gene losses were around 1,000 to 3,000 for L and 4,000 to 6,000 for S, with especially prominent losses in the S subgenome. Many of these losses likely occurred shortly after interspecific hybridization in both L/S subgenomes. We also deduced frequent large inversions in the S subgenome. Upon reassessing transposon dynamics using updated genome databases, we reaffirmed heightened DNA transposon activity during the hybridization, as previously reported. We next investigated whether S subgenome-biased DNA loss could be correlated with the activation of DNA transposons following hybridization. Notably, distinct patterns were observed in the dynamics of DNA transposons between the L and S subgenomes. Several DNA transposon subfamilies correlated positively with DNA deletions in the S subgenome and negatively in the L subgenome. Based on these results, we propose a model that, upon and after hybridization between two related diploid Xenopus species, the mixture of their genomes resulted in the derepression of DNA transposons, especially in the S subgenome, leading to selective DNA loss in the S subgenome.

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Species referenced: Xenopus tropicalis Xenopus laevis Xenopus borealis

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	Fig. 1.Predicted number of lost protein-coding genes corresponding to X. tropicalis orthologs in X. laevis and X. borealis L/S subgenomes. The numbers of predicted lost protein-coding genes in the L and S subgenomes are shown in the Xenopus phylogenetic tree.
	Fig. 2.Relationships of orthologous genes among the X. tropicalis genome and the two subgenomes of X. laevis L/S, X. borealis L/S, X. laevis/X. borealis L, or X. laevis/X. borealis S. The locations of L/S-common, S-specific, and L-specific chromosomal inversions are depicted on the X. tropicalis genome.
	Fig. 3.Scatter plot illustrating the relationship between DNA loss and the amount of transposons in X. laevis, characterized by the slope of the approximation straight line and the correlation coefficient. The values were determined by plotting the ratio of the decreased amount of DNA on each X. laevis chromosome relative to its corresponding X. tropicalis chromosome against the increased amount of each transposon subfamily on the chromosome. DNA fragments from each transposon subfamily were selected with a substitution rate between 0.04 and 0.05. Light and dark dots represent subfamilies from DNA transposons and retrotransposons, respectively.
	Fig. 4.Proposal model for the asymmetric evolution of the L/S subgenome after Xenopus frog hybridization.
	Supplementary Fig. S1. Percentage of DNA components to (sub)genomes across the three Xenopus species.
	Supplementary Fig. S2. Diagram of chromosomal inversions among three Xenopus frogs. Created based on orthologous relationships, it served as the basis for creating Fig. 2.
	Supplementary Fig. S3. Landscapes of DNA transposons and retrotransposons in the three Xenopus species sourced from Xenbase. The substitution ratios for DNA transposons (in blue) and retrotransposons (in red) in X. tropicalis (A), X. laevis L and S (B), and X. borealis L and S (C) are displayed on the horizontal axis. The proportion (%) of transposons relative to each genome's DNA is indicated on the vertical axis. The number 17 represents the speciation and hybridization time (Mya) for the predicted L and S species, corresponding to a substitution ratio of 0.05.
	Supplementary Fig. S4. Scatter plot illustrating the relationship between DNA loss and the amount of transposons in X. laevis, characterized by the slope of the approximation straight line and the correlation coefficient. The values were determined by plotting the ratio of the decreased amount of DNA on each X. laevis chromosome relative to its corresponding X. tropicalis chromosome against the increased amount of each transposon subfamily on the chromosome. DNA fragments from each transposon subfamily were selected with a substitution rate between 0.05. Blue and red dots represent subfamilies from DNA transposons and retrotransposons, respectively.