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Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing

A major threat to rice production is the disease epidemics caused by insect-borne viruses that emerge and re-emerge with undefined origins. It is well known that some human viruses have zoonotic origins from wild animals. However, it remains unknown whether native plants host uncharacterized endemic...

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Autores principales: Yan, Wenkai, Zhu, Yu, Liu, Wencheng, Zou, Chengwu, Jia, Bei, Chen, Zhong-Qi, Han, Yanhong, Wu, Jianguo, Yang, Dong-Lei, Zhang, Zhongkai, Xie, Lianhui, Chen, Baoshan, Li, Rongbai, Ding, Shou-Wei, Wu, Qingfa, Guo, Zhongxin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10076042/
https://www.ncbi.nlm.nih.gov/pubmed/36961862
http://dx.doi.org/10.1371/journal.ppat.1011238
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author Yan, Wenkai
Zhu, Yu
Liu, Wencheng
Zou, Chengwu
Jia, Bei
Chen, Zhong-Qi
Han, Yanhong
Wu, Jianguo
Yang, Dong-Lei
Zhang, Zhongkai
Xie, Lianhui
Chen, Baoshan
Li, Rongbai
Ding, Shou-Wei
Wu, Qingfa
Guo, Zhongxin
author_facet Yan, Wenkai
Zhu, Yu
Liu, Wencheng
Zou, Chengwu
Jia, Bei
Chen, Zhong-Qi
Han, Yanhong
Wu, Jianguo
Yang, Dong-Lei
Zhang, Zhongkai
Xie, Lianhui
Chen, Baoshan
Li, Rongbai
Ding, Shou-Wei
Wu, Qingfa
Guo, Zhongxin
author_sort Yan, Wenkai
collection PubMed
description A major threat to rice production is the disease epidemics caused by insect-borne viruses that emerge and re-emerge with undefined origins. It is well known that some human viruses have zoonotic origins from wild animals. However, it remains unknown whether native plants host uncharacterized endemic viruses with spillover potential to rice (Oryza sativa) as emerging pathogens. Here, we discovered rice tiller inhibition virus (RTIV), a novel RNA virus species, from colonies of Asian wild rice (O. rufipogon) in a genetic reserve by metagenomic sequencing. We identified the specific aphid vector that is able to transmit RTIV and found that RTIV would cause low-tillering disease in rice cultivar after transmission. We further demonstrated that an infectious molecular clone of RTIV initiated systemic infection and causes low-tillering disease in an elite rice variety after Agrobacterium-mediated inoculation or stable plant transformation, and RTIV can also be transmitted from transgenic rice plant through its aphid vector to cause disease. Finally, global transcriptome analysis indicated that RTIV may disturb defense and tillering pathway to cause low tillering disease in rice cultivar. Thus, our results show that new rice viral pathogens can emerge from native habitats, and RTIV, a rare aphid-transmitted rice viral pathogen from native wild rice, can threaten the production of rice cultivar after spillover.
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spelling pubmed-100760422023-04-06 Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing Yan, Wenkai Zhu, Yu Liu, Wencheng Zou, Chengwu Jia, Bei Chen, Zhong-Qi Han, Yanhong Wu, Jianguo Yang, Dong-Lei Zhang, Zhongkai Xie, Lianhui Chen, Baoshan Li, Rongbai Ding, Shou-Wei Wu, Qingfa Guo, Zhongxin PLoS Pathog Research Article A major threat to rice production is the disease epidemics caused by insect-borne viruses that emerge and re-emerge with undefined origins. It is well known that some human viruses have zoonotic origins from wild animals. However, it remains unknown whether native plants host uncharacterized endemic viruses with spillover potential to rice (Oryza sativa) as emerging pathogens. Here, we discovered rice tiller inhibition virus (RTIV), a novel RNA virus species, from colonies of Asian wild rice (O. rufipogon) in a genetic reserve by metagenomic sequencing. We identified the specific aphid vector that is able to transmit RTIV and found that RTIV would cause low-tillering disease in rice cultivar after transmission. We further demonstrated that an infectious molecular clone of RTIV initiated systemic infection and causes low-tillering disease in an elite rice variety after Agrobacterium-mediated inoculation or stable plant transformation, and RTIV can also be transmitted from transgenic rice plant through its aphid vector to cause disease. Finally, global transcriptome analysis indicated that RTIV may disturb defense and tillering pathway to cause low tillering disease in rice cultivar. Thus, our results show that new rice viral pathogens can emerge from native habitats, and RTIV, a rare aphid-transmitted rice viral pathogen from native wild rice, can threaten the production of rice cultivar after spillover. Public Library of Science 2023-03-24 /pmc/articles/PMC10076042/ /pubmed/36961862 http://dx.doi.org/10.1371/journal.ppat.1011238 Text en © 2023 Yan et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Yan, Wenkai
Zhu, Yu
Liu, Wencheng
Zou, Chengwu
Jia, Bei
Chen, Zhong-Qi
Han, Yanhong
Wu, Jianguo
Yang, Dong-Lei
Zhang, Zhongkai
Xie, Lianhui
Chen, Baoshan
Li, Rongbai
Ding, Shou-Wei
Wu, Qingfa
Guo, Zhongxin
Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing
title Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing
title_full Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing
title_fullStr Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing
title_full_unstemmed Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing
title_short Discovery of aphid-transmitted Rice tiller inhibition virus from native plants through metagenomic sequencing
title_sort discovery of aphid-transmitted rice tiller inhibition virus from native plants through metagenomic sequencing
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10076042/
https://www.ncbi.nlm.nih.gov/pubmed/36961862
http://dx.doi.org/10.1371/journal.ppat.1011238
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