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

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

doi:10.1038/s41467-021-24585-9

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

Nat Commun. 2021 Jul 13;12(1):4280. doi: 10.1038/s41467-021-24585-9.

Authors

Shengjun Tan^#^{1

2}, Huijing Ma^#^{1

2

3}, Jinbo Wang^#^{1

2}, Man Wang^#⁴, Mengxia Wang^{1

2

3}, Haodong Yin^{1

3}, Yaqiong Zhang^{1

2}, Xinying Zhang^{1

3}, Jieyu Shen^{1

2

3}, Danyang Wang^{3

5}, Graham L Banes^{6

7}, Zhihua Zhang^{3

5}, Jianmin Wu⁴, Xun Huang^{3

8}, Hua Chen^{3

9

10}, Siqin Ge^{1

3}, Chun-Long Chen^{11

12}, Yong E Zhang^{13

14

15

16

17}

Affiliations

¹ Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
² State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
³ University of Chinese Academy of Sciences, Beijing, China.
⁴ Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Center for Cancer Bioinformatics, Peking University Cancer Hospital & Institute, Beijing, China.
⁵ CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, and China National Center for Bioinformation, Chinese Academy of Sciences, Beijing, China.
⁶ Wisconsin National Primate Research Center, University of Wisconsin-Madison, Madison, WI, USA.
⁷ CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, Chinese Academy of Sciences, Shanghai, China.
⁸ State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China.
⁹ CAS Key Laboratory of Genomics and Precision Medicine, Beijing Institute of Genomics, and China National Center for Bioinformation, Chinese Academy of Sciences, Beijing, China.
¹⁰ CAS Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China.
¹¹ Curie Institute, PSL Research University, CNRS UMR 3244, Paris, France. chunlong.chen@curie.fr.
¹² Sorbonne University, Paris, France. chunlong.chen@curie.fr.
¹³ Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China. zhangyong@ioz.ac.cn.
¹⁴ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China. zhangyong@ioz.ac.cn.
¹⁵ University of Chinese Academy of Sciences, Beijing, China. zhangyong@ioz.ac.cn.
¹⁶ CAS Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China. zhangyong@ioz.ac.cn.
¹⁷ Chinese Institute for Brain Research, Beijing, China. zhangyong@ioz.ac.cn.

^# Contributed equally.

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Animals
DNA Transposable Elements / genetics*
Genome, Plant / genetics*
Oryza / genetics
Terminal Repeat Sequences / genetics*

Substances

DNA Transposable Elements

Grants and funding

P51 OD011106/OD/NIH HHS/United States