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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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 |
work_keys_str_mv |
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