A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors

Many plant rhabdoviruses are neurotropic and can persistently infect the central nervous system (CNS) of their insect vectors without causing significant cytopathology. The mechanisms by which the insect CNS resists infection by plant rhabdoviruses are largely unknown. Here, we report that the neura...

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Main Authors: Haitao Wang, Ye Liu, Lining Mo, Chenyang Huo, Ziyao Wang, Panpan Zhong, Dongsheng Jia, Xiaofeng Zhang, Qian Chen, Hongyan Chen, Taiyun Wei
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00513/full
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spelling doaj-57bf86ee212c493c925d98c60c4c4f5b2020-11-25T03:16:36ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-04-011110.3389/fmicb.2020.00513522440A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper VectorsHaitao WangYe LiuLining MoChenyang HuoZiyao WangPanpan ZhongDongsheng JiaXiaofeng ZhangQian ChenHongyan ChenTaiyun WeiMany plant rhabdoviruses are neurotropic and can persistently infect the central nervous system (CNS) of their insect vectors without causing significant cytopathology. The mechanisms by which the insect CNS resists infection by plant rhabdoviruses are largely unknown. Here, we report that the neural factor Hikaru genki homolog of the leafhopper Nephotettix cincticeps (NcHig) limits the spread of the nucleorhabdovirus rice yellow stunt virus (RYSV) in vector CNS. NcHig is predominantly expressed in the CNS of N. cincticeps, and the knockdown of NcHig expression by RNA interference enhances RYSV infection of the CNS. Furthermore, immuno-blockade of NcHig function by microinjection of N. cincticeps with NcHig antibody also enhances viral infection of the CNS. Thus, we conclude that the neuron-specific factor NcHig can control RYSV propagation in the CNS. Interestingly, we find the Hig homolog of the leafhopper Recilia dorsalis also has antiviral activity during the persistent infection of the cytorhabdovirus rice stripe mosaic virus (RSMV) in vector CNS. We further determine that RYSV and RSMV matrix proteins specifically interact with the complement control protein (CCP) domains of Higs. Thus, the matrix protein-binding ability of Hig is potentially essential for its antiviral activity in rice leafhoppers. Our results demonstrate an evolutionarily conserved antiviral mechanism for Hig to mediate the persistent infection of rice rhabdoviruses in the CNS of leafhopper vectors.https://www.frontiersin.org/article/10.3389/fmicb.2020.00513/fullantiviral mechanismcentral nervous systemHikaru genkirice rhabdovirusesrice leafhopperrice yellow stunt virus
collection DOAJ
language English
format Article
sources DOAJ
author Haitao Wang
Ye Liu
Lining Mo
Chenyang Huo
Ziyao Wang
Panpan Zhong
Dongsheng Jia
Xiaofeng Zhang
Qian Chen
Hongyan Chen
Taiyun Wei
spellingShingle Haitao Wang
Ye Liu
Lining Mo
Chenyang Huo
Ziyao Wang
Panpan Zhong
Dongsheng Jia
Xiaofeng Zhang
Qian Chen
Hongyan Chen
Taiyun Wei
A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors
Frontiers in Microbiology
antiviral mechanism
central nervous system
Hikaru genki
rice rhabdoviruses
rice leafhopper
rice yellow stunt virus
author_facet Haitao Wang
Ye Liu
Lining Mo
Chenyang Huo
Ziyao Wang
Panpan Zhong
Dongsheng Jia
Xiaofeng Zhang
Qian Chen
Hongyan Chen
Taiyun Wei
author_sort Haitao Wang
title A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors
title_short A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors
title_full A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors
title_fullStr A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors
title_full_unstemmed A Neuron-Specific Antiviral Mechanism Modulates the Persistent Infection of Rice Rhabdoviruses in Leafhopper Vectors
title_sort neuron-specific antiviral mechanism modulates the persistent infection of rice rhabdoviruses in leafhopper vectors
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-04-01
description Many plant rhabdoviruses are neurotropic and can persistently infect the central nervous system (CNS) of their insect vectors without causing significant cytopathology. The mechanisms by which the insect CNS resists infection by plant rhabdoviruses are largely unknown. Here, we report that the neural factor Hikaru genki homolog of the leafhopper Nephotettix cincticeps (NcHig) limits the spread of the nucleorhabdovirus rice yellow stunt virus (RYSV) in vector CNS. NcHig is predominantly expressed in the CNS of N. cincticeps, and the knockdown of NcHig expression by RNA interference enhances RYSV infection of the CNS. Furthermore, immuno-blockade of NcHig function by microinjection of N. cincticeps with NcHig antibody also enhances viral infection of the CNS. Thus, we conclude that the neuron-specific factor NcHig can control RYSV propagation in the CNS. Interestingly, we find the Hig homolog of the leafhopper Recilia dorsalis also has antiviral activity during the persistent infection of the cytorhabdovirus rice stripe mosaic virus (RSMV) in vector CNS. We further determine that RYSV and RSMV matrix proteins specifically interact with the complement control protein (CCP) domains of Higs. Thus, the matrix protein-binding ability of Hig is potentially essential for its antiviral activity in rice leafhoppers. Our results demonstrate an evolutionarily conserved antiviral mechanism for Hig to mediate the persistent infection of rice rhabdoviruses in the CNS of leafhopper vectors.
topic antiviral mechanism
central nervous system
Hikaru genki
rice rhabdoviruses
rice leafhopper
rice yellow stunt virus
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00513/full
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