Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper Vector

Melanization in the hemolymph of arthropods is a conserved defense strategy against infection by invading pathogens. Numerous plant viruses are persistently transmitted by insect vectors, and must overcome hemolymph melanization. Here, we determine that the plant rhabdovirus rice stripe mosaic virus...

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Main Authors: Ruonan Zhang, Xiao-Feng Zhang, Yunhua Chi, Yuanyuan Xu, Hongyan Chen, Zhongxin Guo, Taiyun Wei
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.904244/full
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author Ruonan Zhang
Xiao-Feng Zhang
Yunhua Chi
Yuanyuan Xu
Hongyan Chen
Zhongxin Guo
Taiyun Wei
author_facet Ruonan Zhang
Xiao-Feng Zhang
Yunhua Chi
Yuanyuan Xu
Hongyan Chen
Zhongxin Guo
Taiyun Wei
author_sort Ruonan Zhang
collection DOAJ
description Melanization in the hemolymph of arthropods is a conserved defense strategy against infection by invading pathogens. Numerous plant viruses are persistently transmitted by insect vectors, and must overcome hemolymph melanization. Here, we determine that the plant rhabdovirus rice stripe mosaic virus (RSMV) has evolved to evade the antiviral melanization response in the hemolymph in leafhopepr vectors. After virions enter vector hemolymph cells, viral nucleoprotein N is initially synthesized and directly interacts with prophenoloxidase (PPO), a core component of the melanization pathway and this process strongly activates the expression of PPO. Furthermore, such interaction could effectively inhibit the proteolytic cleavage of the zymogen PPO to active phenoloxidase (PO), finally suppressing hemolymph melanization. The knockdown of PPO expression or treatment with the PO inhibitor also suppresses hemolymph melanization and causes viral excessive accumulation, finally causing a high insect mortality rate. Consistent with this function, microinjection of N into leafhopper vectors attenuates melanization and promotes viral infection. These findings demonstrate that RSMV N serves as the effector to attenuate hemolymph melanization and facilitate viral persistent propagation in its insect vector. Our findings provide the insights in the understanding of ongoing arms race of insect immunity defense and viral counter-defense.
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spelling doaj.art-04acdc92138444ca89ed448b0d6b05682022-12-22T03:34:15ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-05-011310.3389/fimmu.2022.904244904244Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper VectorRuonan ZhangXiao-Feng ZhangYunhua ChiYuanyuan XuHongyan ChenZhongxin GuoTaiyun WeiMelanization in the hemolymph of arthropods is a conserved defense strategy against infection by invading pathogens. Numerous plant viruses are persistently transmitted by insect vectors, and must overcome hemolymph melanization. Here, we determine that the plant rhabdovirus rice stripe mosaic virus (RSMV) has evolved to evade the antiviral melanization response in the hemolymph in leafhopepr vectors. After virions enter vector hemolymph cells, viral nucleoprotein N is initially synthesized and directly interacts with prophenoloxidase (PPO), a core component of the melanization pathway and this process strongly activates the expression of PPO. Furthermore, such interaction could effectively inhibit the proteolytic cleavage of the zymogen PPO to active phenoloxidase (PO), finally suppressing hemolymph melanization. The knockdown of PPO expression or treatment with the PO inhibitor also suppresses hemolymph melanization and causes viral excessive accumulation, finally causing a high insect mortality rate. Consistent with this function, microinjection of N into leafhopper vectors attenuates melanization and promotes viral infection. These findings demonstrate that RSMV N serves as the effector to attenuate hemolymph melanization and facilitate viral persistent propagation in its insect vector. Our findings provide the insights in the understanding of ongoing arms race of insect immunity defense and viral counter-defense.https://www.frontiersin.org/articles/10.3389/fimmu.2022.904244/fullrice stripe mosaic virusmelanizationleafhopperprophenoloxidases (PPO)viral infection
spellingShingle Ruonan Zhang
Xiao-Feng Zhang
Yunhua Chi
Yuanyuan Xu
Hongyan Chen
Zhongxin Guo
Taiyun Wei
Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper Vector
Frontiers in Immunology
rice stripe mosaic virus
melanization
leafhopper
prophenoloxidases (PPO)
viral infection
title Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper Vector
title_full Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper Vector
title_fullStr Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper Vector
title_full_unstemmed Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper Vector
title_short Nucleoprotein of a Rice Rhabdovirus Serves as the Effector to Attenuate Hemolymph Melanization and Facilitate Viral Persistent Propagation in its Leafhopper Vector
title_sort nucleoprotein of a rice rhabdovirus serves as the effector to attenuate hemolymph melanization and facilitate viral persistent propagation in its leafhopper vector
topic rice stripe mosaic virus
melanization
leafhopper
prophenoloxidases (PPO)
viral infection
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.904244/full
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