Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem

Numerous piercing-sucking insects can horizontally transmit viral pathogens together with saliva to plant phloem, but the mechanism remains elusive. Here, we report that an important rice reovirus has hijacked small vesicles, referred to as exosomes, to traverse the apical plasmalemma into saliva-st...

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Main Authors: Qian Chen, Yuyan Liu, Jiping Ren, Panpan Zhong, Manni Chen, Dongsheng Jia, Hongyan Chen, Taiyun Wei
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-07-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/64603
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spelling doaj-9519f10c1ba748428a813d7a1dcdc6c42021-07-02T16:43:12ZengeLife Sciences Publications LtdeLife2050-084X2021-07-011010.7554/eLife.64603Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloemQian Chen0https://orcid.org/0000-0002-8442-6089Yuyan Liu1Jiping Ren2Panpan Zhong3Manni Chen4Dongsheng Jia5Hongyan Chen6Taiyun Wei7https://orcid.org/0000-0002-0732-9752Vector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaVector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaVector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaVector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaVector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaVector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaVector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaVector-borne Virus Research Center, Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, ChinaNumerous piercing-sucking insects can horizontally transmit viral pathogens together with saliva to plant phloem, but the mechanism remains elusive. Here, we report that an important rice reovirus has hijacked small vesicles, referred to as exosomes, to traverse the apical plasmalemma into saliva-stored cavities in the salivary glands of leafhopper vectors. Thus, virions were horizontally transmitted with exosomes into rice phloem to establish the initial plant infection during vector feeding. The purified exosomes secreted from cultured leafhopper cells were enriched with virions. Silencing the exosomal secretion-related small GTPase Rab27a or treatment with the exosomal biogenesis inhibitor GW4869 strongly prevented viral exosomal release in vivo and in vitro. Furthermore, the specific interaction of the 15-nm-long domain of the viral outer capsid protein with Rab5 induced the packaging of virions in exosomes, ultimately activating the Rab27a-dependent exosomal release pathway. We thus anticipate that exosome-mediated viral horizontal transmission is the conserved strategy hijacked by vector-borne viruses.https://elifesciences.org/articles/64603exosomemultivesicular bodiesinsect vectorssalivary glandsviral transmissionplant phloem
collection DOAJ
language English
format Article
sources DOAJ
author Qian Chen
Yuyan Liu
Jiping Ren
Panpan Zhong
Manni Chen
Dongsheng Jia
Hongyan Chen
Taiyun Wei
spellingShingle Qian Chen
Yuyan Liu
Jiping Ren
Panpan Zhong
Manni Chen
Dongsheng Jia
Hongyan Chen
Taiyun Wei
Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem
eLife
exosome
multivesicular bodies
insect vectors
salivary glands
viral transmission
plant phloem
author_facet Qian Chen
Yuyan Liu
Jiping Ren
Panpan Zhong
Manni Chen
Dongsheng Jia
Hongyan Chen
Taiyun Wei
author_sort Qian Chen
title Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem
title_short Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem
title_full Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem
title_fullStr Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem
title_full_unstemmed Exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem
title_sort exosomes mediate horizontal transmission of viral pathogens from insect vectors to plant phloem
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-07-01
description Numerous piercing-sucking insects can horizontally transmit viral pathogens together with saliva to plant phloem, but the mechanism remains elusive. Here, we report that an important rice reovirus has hijacked small vesicles, referred to as exosomes, to traverse the apical plasmalemma into saliva-stored cavities in the salivary glands of leafhopper vectors. Thus, virions were horizontally transmitted with exosomes into rice phloem to establish the initial plant infection during vector feeding. The purified exosomes secreted from cultured leafhopper cells were enriched with virions. Silencing the exosomal secretion-related small GTPase Rab27a or treatment with the exosomal biogenesis inhibitor GW4869 strongly prevented viral exosomal release in vivo and in vitro. Furthermore, the specific interaction of the 15-nm-long domain of the viral outer capsid protein with Rab5 induced the packaging of virions in exosomes, ultimately activating the Rab27a-dependent exosomal release pathway. We thus anticipate that exosome-mediated viral horizontal transmission is the conserved strategy hijacked by vector-borne viruses.
topic exosome
multivesicular bodies
insect vectors
salivary glands
viral transmission
plant phloem
url https://elifesciences.org/articles/64603
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AT panpanzhong exosomesmediatehorizontaltransmissionofviralpathogensfrominsectvectorstoplantphloem
AT mannichen exosomesmediatehorizontaltransmissionofviralpathogensfrominsectvectorstoplantphloem
AT dongshengjia exosomesmediatehorizontaltransmissionofviralpathogensfrominsectvectorstoplantphloem
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