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...
Main Authors: | , , , , , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Nature Portfolio
2023-11-01
|
Series: | Nature Communications |
Online Access: | https://doi.org/10.1038/s41467-023-43186-2 |
_version_ | 1797630081069219840 |
---|---|
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. |
first_indexed | 2024-03-11T11:02:56Z |
format | Article |
id | doaj.art-15bd8121d1db4cefbed53556eb548424 |
institution | Directory Open Access Journal |
issn | 2041-1723 |
language | English |
last_indexed | 2024-03-11T11:02:56Z |
publishDate | 2023-11-01 |
publisher | Nature Portfolio |
record_format | Article |
series | Nature Communications |
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 |
work_keys_str_mv | AT haijianhuang cooptionofanonretroviralendogenousviralelementinplanthoppers AT yiyuanli cooptionofanonretroviralendogenousviralelementinplanthoppers AT zhuangxinye cooptionofanonretroviralendogenousviralelementinplanthoppers AT lilili cooptionofanonretroviralendogenousviralelementinplanthoppers AT qinglinghu cooptionofanonretroviralendogenousviralelementinplanthoppers AT yujuanhe cooptionofanonretroviralendogenousviralelementinplanthoppers AT yuhuaqi cooptionofanonretroviralendogenousviralelementinplanthoppers AT yanzhang cooptionofanonretroviralendogenousviralelementinplanthoppers AT tingli cooptionofanonretroviralendogenousviralelementinplanthoppers AT ganglu cooptionofanonretroviralendogenousviralelementinplanthoppers AT qianzhuomao cooptionofanonretroviralendogenousviralelementinplanthoppers AT jichongzhuo cooptionofanonretroviralendogenousviralelementinplanthoppers AT jiabaolu cooptionofanonretroviralendogenousviralelementinplanthoppers AT zhongtianxu cooptionofanonretroviralendogenousviralelementinplanthoppers AT zongtaosun cooptionofanonretroviralendogenousviralelementinplanthoppers AT feiyan cooptionofanonretroviralendogenousviralelementinplanthoppers AT jianpingchen cooptionofanonretroviralendogenousviralelementinplanthoppers AT chuanxizhang cooptionofanonretroviralendogenousviralelementinplanthoppers AT junminli cooptionofanonretroviralendogenousviralelementinplanthoppers |