Comprehensive analysis of the Xya riparia genome uncovers the dominance of DNA transposons, LTR/Gypsy elements, and their evolutionary dynamics

Abstract

Transposable elements (TEs) are DNA sequences that can move or replicate within a genome, and their study has become increasingly important in understanding genome evolution and function. The Tridactylidae family, including Xya riparia (pygmy mole cricket), harbors a variety of transposable elements (TEs) that have been insufficiently investigated. Further research is required to fully understand their diversity and evolutionary characteristics. Hence, we conducted a comprehensive repeatome analysis of X. riparia species using the chromosome-level assembled genome. The study aimed to comprehensively analyze the abundance, distribution, and age of transposable elements (TEs) in the genome. The results indicated that the genome was 1.67 Gb, with 731.63 Mb of repetitive sequences, comprising 27% of Class II (443.25 Mb), 16% of Class I (268.45 Mb), and 1% of unknown TEs (19.92 Mb). The study found that DNA transposons dominate the genome, accounting for approximately 60% of the total repeat size, with retrotransposons and unknown elements accounting for 37% and 3% of the genome, respectively. The members of the Gypsy superfamily were the most abundant amongst retrotransposons, accounting for 63% of them. The transposable superfamilies (LTR/Gypsy, DNA/nMITE, DNA/hAT, and DNA/Helitron) collectively constituted almost 70% of the total repeat size of all six chromosomes. The study further unveiled a significant linear correlation (Pearson correlation: r = 0.99, p-value = 0.00003) between the size of the chromosomes and the repetitive sequences. The average age of DNA transposon and retrotransposon insertions ranges from 25 My (million years) to 5 My. The satellitome analysis discovered 13 satellite DNA families that comprise about 0.15% of the entire genome. In addition, the transcriptional analysis of TEs found that DNA transposons were more transcriptionally active than retrotransposons. Overall, the study suggests that the genome of X. riparia is complex, characterized by a substantial portion of repetitive elements. These findings not only enhance our understanding of TE evolution within the Tridactylidae family but also provide a foundation for future investigations into the genomic intricacies of related species.

Keywords: Age analysis; Orthoptera; Pygmy mole crickets; Transposable elements.

Fig. 1

The complete genome analysis of transposable elements (TEs). The genome was divided into two parts - one representing the proportion of repetitive sequences and the other representing coding or single-copy sequences (shown on the left). The right-side graph shows the total size (in Mb) of each superfamily in the genome. The x-axis indicates the name of each family, while the y-axis represents the size of the TEs in megabase pairs (Mbp) (right)

Fig. 2

Superfamilies-level Transposable elements annotation of six X. riparia chromosomes. Abundance and distribution comparison of transposable elements across six chromosomes

Fig. 3

The evolutionary landscape of transposable elements (TEs) in X. riparia. The graph displays the proportion of the genome (%) on the y-axis and the degree of divergence based on the kimura distance on the x-axis. The K values range from 1 to 50, indicating the level of evolutionary divergence from younger to older TEs

Fig. 4

Class I superfamilies insertion times and relative abundance across the chromosomes. The TE distribution patterns are illustrated in the “1 My (million years)” bins on the x-axis. The proportion of the genome occupied by TEs is depicted on the y-axis, which is determined using the RepeatMasker align output

Fig. 5

Class II superfamilies insertion times across the chromosomes. The TE distribution patterns are illustrated in the “1 My (million years)” bins on the x-axis. The proportion of the genome occupied by TEs is depicted on the y-axis, which is determined using the RepeatMasker align output

Fig. 6

LTR/Gypsy subfamilies abundance and divergence repeat graphs. The x-axis depicts the degree of divergence, while the y-axis represents the total genome proportion. The graphs’ peaks indicate the insertion times of a particular subfamily in the genome. The graph’s right side indicates elements inserted earlier in the genome, whereas the left indicates recent insertions

Fig. 7

TIR subfamilies abundance and divergence repeat graphs. The x-axis depicts the degree of divergence, while the y-axis represents the total genome proportion. The graphs’ peaks indicate the insertion times of a particular subfamily in the genome. The graph’s right side indicates elements inserted earlier in the genome, whereas the left indicates recent insertions

Fig. 8

The graphs illustrate the relationship between the genome percentage and the sequence divergence of each satellite DNA family across the chromosomes. The x-axis represents the degree of divergence from the consensus sequence of the elements, while the y-axis indicates the number of copies present in the genome. Peaks on the graphs show times of insertions of a specific family in the genome. The elements inserted in the genome earlier are found on the right side of the graph, while recent insertions are on the left

Fig. 9

A visual representation of a heatmap illustrates the expression of 48 subfamilies of transposable elements that are differentially expressed across two samples of X. riparia