Co-option of a non-retroviral endogenous viral element in planthoppers

Hai-Jian Huang; Yi-Yuan Li; Zhuang-Xin Ye; Li-Li Li; Qing-Ling Hu; Yu-Juan He; Yu-Hua Qi; Yan Zhang; Ting Li; Gang Lu; Qian-Zhuo Mao; Ji-Chong Zhuo; Jia-Bao Lu; Zhong-Tian Xu; Zong-Tao Sun; Fei Yan; Jian-Ping Chen; Chuan-Xi Zhang; Jun-Min Li

doi:10.1038/s41467-023-43186-2

Co-option of a non-retroviral endogenous viral element in planthoppers

Nat Commun. 2023 Nov 9;14(1):7264. doi: 10.1038/s41467-023-43186-2.

Authors

Hai-Jian Huang^{1

2}, Yi-Yuan Li^{1

2}, Zhuang-Xin Ye^{1

2

3}, Li-Li Li^{1

2}, Qing-Ling Hu^{1

2}, Yu-Juan He^{1

2}, Yu-Hua Qi^{1

2}, Yan Zhang^{1

2}, Ting Li^{1

2}, Gang Lu^{1

2}, Qian-Zhuo Mao^{1

2}, Ji-Chong Zhuo^{1

2}, Jia-Bao Lu^{1

2}, Zhong-Tian Xu^{1

2}, Zong-Tao Sun^{1

2}, Fei Yan^{1

2}, Jian-Ping Chen^{4

5

6}, Chuan-Xi Zhang^{7

8}, Jun-Min Li^{9

10}

Affiliations

¹ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.
² Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China.
³ College of Forestry, Nanjing Forestry University, Nanjing, 210037, China.
⁴ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. jianpingchen@nbu.edu.cn.
⁵ Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. jianpingchen@nbu.edu.cn.
⁶ College of Forestry, Nanjing Forestry University, Nanjing, 210037, China. jianpingchen@nbu.edu.cn.
⁷ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. chxzhang@zju.edu.cn.
⁸ Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. chxzhang@zju.edu.cn.
⁹ State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. lijunmin@nbu.edu.cn.
¹⁰ Key Laboratory of Biotechnology in Plant Protection of Ministry of Agriculture and Zhejiang Province, Institute of Plant Virology, Ningbo University, Ningbo, 315211, China. lijunmin@nbu.edu.cn.

Abstract

Non-retroviral endogenous viral elements (nrEVEs) are widely dispersed throughout the genomes of eukaryotes. Although nrEVEs are known to be involved in host antiviral immunity, it remains an open question whether they can be domesticated as functional proteins to serve cellular innovations in arthropods. In this study, we found that endogenous toti-like viral elements (ToEVEs) are ubiquitously integrated into the genomes of three planthopper species, with highly variable distributions and polymorphism levels in planthopper populations. Three ToEVEs display exon‒intron structures and active transcription, suggesting that they might have been domesticated by planthoppers. CRISPR/Cas9 experiments revealed that one ToEVE in Nilaparvata lugens, NlToEVE14, has been co-opted by its host and plays essential roles in planthopper development and fecundity. Large-scale analysis of ToEVEs in arthropod genomes indicated that the number of arthropod nrEVEs is currently underestimated and that they may contribute to the functional diversity of arthropod genes.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Arthropods* / genetics
Hemiptera* / genetics
Retroviridae