Leafhopper salivary vitellogenin mediates virus transmission to plant phloem

Abstract Salivary effectors of piercing-sucking insects can suppress plant defense to promote insect feeding, but it remains largely elusive how they facilitate plant virus transmission. Leafhopper Nephotettix cincticeps transmits important rice reovirus via virus-packaging exosomes released from sa...

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Main Authors: Yanfei Wang, Chengcong Lu, Shude Guo, Yuxin Guo, Taiyun Wei, Qian Chen
Format: Article
Language:English
Published: Nature Portfolio 2024-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-43488-5
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author Yanfei Wang
Chengcong Lu
Shude Guo
Yuxin Guo
Taiyun Wei
Qian Chen
author_facet Yanfei Wang
Chengcong Lu
Shude Guo
Yuxin Guo
Taiyun Wei
Qian Chen
author_sort Yanfei Wang
collection DOAJ
description Abstract Salivary effectors of piercing-sucking insects can suppress plant defense to promote insect feeding, but it remains largely elusive how they facilitate plant virus transmission. Leafhopper Nephotettix cincticeps transmits important rice reovirus via virus-packaging exosomes released from salivary glands and then entering the rice phloem. Here, we report that intact salivary vitellogenin of N. cincticeps (NcVg) is associated with the GTPase Rab5 of N. cincticeps (NcRab5) for release from salivary glands. In virus-infected salivary glands, NcVg is upregulated and packaged into exosomes mediated by virus-induced NcRab5, subsequently entering the rice phloem. The released NcVg inherently suppresses H2O2 burst of rice plants by interacting with rice glutathione S-transferase F12, an enzyme catalyzing glutathione-dependent oxidation, thus facilitating leafhoppers feeding. When leafhoppers transmit virus, virus-upregulated NcVg thus promotes leafhoppers feeding and enhances viral transmission. Taken together, the findings provide evidence that viruses exploit insect exosomes to deliver virus-hijacked effectors for efficient transmission.
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spelling doaj.art-629cbbcc2b554ad980510efa3be5963f2024-01-07T12:32:30ZengNature PortfolioNature Communications2041-17232024-01-0115111910.1038/s41467-023-43488-5Leafhopper salivary vitellogenin mediates virus transmission to plant phloemYanfei Wang0Chengcong Lu1Shude Guo2Yuxin Guo3Taiyun Wei4Qian Chen5Vector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry UniversityVector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry UniversityVector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry UniversityVector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry UniversityVector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry UniversityVector-borne Virus Research Center, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry UniversityAbstract Salivary effectors of piercing-sucking insects can suppress plant defense to promote insect feeding, but it remains largely elusive how they facilitate plant virus transmission. Leafhopper Nephotettix cincticeps transmits important rice reovirus via virus-packaging exosomes released from salivary glands and then entering the rice phloem. Here, we report that intact salivary vitellogenin of N. cincticeps (NcVg) is associated with the GTPase Rab5 of N. cincticeps (NcRab5) for release from salivary glands. In virus-infected salivary glands, NcVg is upregulated and packaged into exosomes mediated by virus-induced NcRab5, subsequently entering the rice phloem. The released NcVg inherently suppresses H2O2 burst of rice plants by interacting with rice glutathione S-transferase F12, an enzyme catalyzing glutathione-dependent oxidation, thus facilitating leafhoppers feeding. When leafhoppers transmit virus, virus-upregulated NcVg thus promotes leafhoppers feeding and enhances viral transmission. Taken together, the findings provide evidence that viruses exploit insect exosomes to deliver virus-hijacked effectors for efficient transmission.https://doi.org/10.1038/s41467-023-43488-5
spellingShingle Yanfei Wang
Chengcong Lu
Shude Guo
Yuxin Guo
Taiyun Wei
Qian Chen
Leafhopper salivary vitellogenin mediates virus transmission to plant phloem
Nature Communications
title Leafhopper salivary vitellogenin mediates virus transmission to plant phloem
title_full Leafhopper salivary vitellogenin mediates virus transmission to plant phloem
title_fullStr Leafhopper salivary vitellogenin mediates virus transmission to plant phloem
title_full_unstemmed Leafhopper salivary vitellogenin mediates virus transmission to plant phloem
title_short Leafhopper salivary vitellogenin mediates virus transmission to plant phloem
title_sort leafhopper salivary vitellogenin mediates virus transmission to plant phloem
url https://doi.org/10.1038/s41467-023-43488-5
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