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

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...

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Main Authors: 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
Format: Article
Language:English
Published: Nature Portfolio 2023-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-43186-2
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author 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
author_facet 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
author_sort Hai-Jian Huang
collection DOAJ
description 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.
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spelling doaj.art-15bd8121d1db4cefbed53556eb5484242023-11-12T12:23:06ZengNature PortfolioNature Communications2041-17232023-11-0114111910.1038/s41467-023-43186-2Co-option of a non-retroviral endogenous viral element in planthoppersHai-Jian Huang0Yi-Yuan Li1Zhuang-Xin Ye2Li-Li Li3Qing-Ling Hu4Yu-Juan He5Yu-Hua Qi6Yan Zhang7Ting Li8Gang Lu9Qian-Zhuo Mao10Ji-Chong Zhuo11Jia-Bao Lu12Zhong-Tian Xu13Zong-Tao Sun14Fei Yan15Jian-Ping Chen16Chuan-Xi Zhang17Jun-Min Li18State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Institute of Plant Virology, Ningbo UniversityAbstract 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.https://doi.org/10.1038/s41467-023-43186-2
spellingShingle 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
Co-option of a non-retroviral endogenous viral element in planthoppers
Nature Communications
title Co-option of a non-retroviral endogenous viral element in planthoppers
title_full Co-option of a non-retroviral endogenous viral element in planthoppers
title_fullStr Co-option of a non-retroviral endogenous viral element in planthoppers
title_full_unstemmed Co-option of a non-retroviral endogenous viral element in planthoppers
title_short Co-option of a non-retroviral endogenous viral element in planthoppers
title_sort co option of a non retroviral endogenous viral element in planthoppers
url https://doi.org/10.1038/s41467-023-43186-2
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