DNA transposons mediate duplications via transposition-independent and -dependent mechanisms in metazoans

Shengjun Tan,Hua Chen,Mengxia Wang,Zhihua Zhang,Yaqiong Zhang,Yong E Zhang,Graham L Banes,Man Wang,Xinying Zhang,Chun-Long Chen,Jianmin Wu,Siqin Ge,Huijing Ma,Jieyu Shen,Jinbo Wang,Xun Huang,Danyang Wang,Haodong Yin

doi:10.1038/s41467-021-24585-9

Abstract

Despite long being considered as “junk”, transposable elements (TEs) are now accepted as catalysts of evolution. One example is Mutator-like elements (MULEs, one type of terminal inverted repeat DNA TEs, or TIR TEs) capturing sequences as Pack-MULEs in plants. However, their origination mechanism remains perplexing, and whether TIR TEs mediate duplication in animals is almost unexplored. Here we identify 370 Pack-TIRs in 100 animal reference genomes and one Pack-TIR (Ssk-FB4) family in fly populations. We find that single-copy Pack-TIRs are mostly generated via transposition-independent gap filling, and multicopy Pack-TIRs are likely generated by transposition after replication fork switching. We show that a proportion of Pack-TIRs are transcribed and often form chimeras with hosts. We also find that Ssk-FB4s represent a young protein family, as supported by proteomics and signatures of positive selection. Thus, TIR TEs catalyze new gene structures and new genes in animals via both transposition-independent and -dependent mechanisms.

Highlights

Despite long being considered as “junk”, transposable elements (TEs) are accepted as catalysts of evolution
TE called FB4) family in D. melanogaster populations. Sequence analyses of these Pack-TIRs suggest that single-copy Pack-TIRs are mostly generated via a transposition-independent gap-filling process, whereas the birth of multicopy Pack-TIRs is compatible with a new model, which we describe as replication Fork Stalling, Template Switching and Transposition (FoSTeST)
We focused on D. melanogaster given the ease of the experiments and the availability of resequencing data generated with the D. melanogaster Genetic Reference Panel (DGRP)[33], and we identified one multicopy Pack-TIR family, Ssk-FB4s

Summary

Introduction

Despite long being considered as “junk”, transposable elements (TEs) are accepted as catalysts of evolution. One example is Mutator-like elements (MULEs, one type of terminal inverted repeat DNA TEs, or TIR TEs) capturing sequences as Pack-MULEs in plants. Their origination mechanism remains perplexing, and whether TIR TEs mediate duplication in animals is almost unexplored. Among DNA transposons, Helitrons duplicate non-TE sequences in animals and plants[16,17], whereas terminal inverted repeat TE (TIR TE)-. P elements capture sequences under the gap-filling model[21] In this model, double-strand breaks (DSBs) occur in two scenarios: (1) the internal sites are broken, possibly induced by secondary structures[22,23] (Supplementary Fig. 1b); or (2) complete TEs are excised due to transposition[24] (Supplementary Fig. 1c). The whole process in the former scenario (Supplementary Fig. 1b) is transposition-independent

Methods

Results

Conclusion