Activation of DNA Transposons and Evolution of piRNA Genes Through Interspecific Hybridization in Xenopus Frogs.

Kosuke Suda,Kei Tamura,Shun R Hayashi,Nobuhiko Takamatsu,Michihiko Ito

doi:10.3389/fgene.2022.766424

Abstract

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.

Highlights

Interspecific hybridization, which is the crossing of two species, plays an important role in evolution
Predicted PIWI-interacting RNAs (piRNA) molecules were selected from comprehensive sequences of small RNAs from the ovaries and testes of the three Xenopus species (Section 2; Figure 1)
We found that there were more than 107 piRNAs in each gonad from the three species, and more than 90% of the piRNAs were distinct between the ovary and testis from each species (Supplementary Figure S2)

Summary

Introduction

Interspecific hybridization, which is the crossing of two species, plays an important role in evolution. Many events of whole genome duplication (WGD) occurred during interspecific hybridization. Hybridization was believed to be involved in the two-rounds of WGD in the common ancestor of vertebrates (Ohno, 1970; Holland et al, 1994; Spring, 1997). Simakov et al (2020) reported that the second WGD occurred in the mid–late Ordovician by interspecific hybridization. The allotetraploid frog Xenopus laevis diverged from the hybrid between two closely related diploid Xenopus species. Session et al (2016) reported that the allotetraploid X. laevis origin should have had two distinct subgenomes with distinct families of transposable elements (TEs), and that the two diploid progenitor species diverged about 34 million years ago (mya) and hybridized approximately 17–18 mya.

Methods

Results

Conclusion