Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.

Maintenance of a balance between the levels of viral replication and selective pressure from the immune systems of insect vectors is one of the prerequisites for efficient transmission of insect-borne propagative phytoviruses. The mechanism regulating the adaptation of RNA viruses to insect vectors...

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Main Authors: Wan Zhao, Jinting Yu, Feng Jiang, Wei Wang, Le Kang, Feng Cui
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-03-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1009424
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spelling doaj-db2a83d2e61441efa811ce27314552152021-07-28T04:33:15ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742021-03-01173e100942410.1371/journal.ppat.1009424Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.Wan ZhaoJinting YuFeng JiangWei WangLe KangFeng CuiMaintenance of a balance between the levels of viral replication and selective pressure from the immune systems of insect vectors is one of the prerequisites for efficient transmission of insect-borne propagative phytoviruses. The mechanism regulating the adaptation of RNA viruses to insect vectors by genomic variation remains unknown. Our previous study demonstrated an extension of the 3'-untranslated terminal region (UTR) of two genomic segments of rice stripe virus (RSV). In the present study, a reverse genetic system for RSV in human cells and an insect vector, the small brown planthopper Laodelphax striatellus, was used to demonstrate that the 3'-terminal extensions suppressed viral replication in vector insects by inhibiting promoter activity due to structural interference with the panhandle structure formed by viral 3'- and 5'-UTRs. The extension sequence in the viral RNA1 segment was targeted by an endogenous insect microRNA, miR-263a, which decreased the inhibitory effect of the extension sequence on viral promoter activity. Surprisingly, the expression of miR-263a was negatively regulated by RSV infection. This elaborate coordination between terminal variation of the viral genome and endogenous insect microRNAs controls RSV replication in planthopper, thus reflecting a distinct strategy of adaptation of phytoviruses to insect vectors.https://doi.org/10.1371/journal.ppat.1009424
collection DOAJ
language English
format Article
sources DOAJ
author Wan Zhao
Jinting Yu
Feng Jiang
Wei Wang
Le Kang
Feng Cui
spellingShingle Wan Zhao
Jinting Yu
Feng Jiang
Wei Wang
Le Kang
Feng Cui
Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.
PLoS Pathogens
author_facet Wan Zhao
Jinting Yu
Feng Jiang
Wei Wang
Le Kang
Feng Cui
author_sort Wan Zhao
title Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.
title_short Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.
title_full Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.
title_fullStr Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.
title_full_unstemmed Coordination between terminal variation of the viral genome and insect microRNAs regulates rice stripe virus replication in insect vectors.
title_sort coordination between terminal variation of the viral genome and insect micrornas regulates rice stripe virus replication in insect vectors.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2021-03-01
description Maintenance of a balance between the levels of viral replication and selective pressure from the immune systems of insect vectors is one of the prerequisites for efficient transmission of insect-borne propagative phytoviruses. The mechanism regulating the adaptation of RNA viruses to insect vectors by genomic variation remains unknown. Our previous study demonstrated an extension of the 3'-untranslated terminal region (UTR) of two genomic segments of rice stripe virus (RSV). In the present study, a reverse genetic system for RSV in human cells and an insect vector, the small brown planthopper Laodelphax striatellus, was used to demonstrate that the 3'-terminal extensions suppressed viral replication in vector insects by inhibiting promoter activity due to structural interference with the panhandle structure formed by viral 3'- and 5'-UTRs. The extension sequence in the viral RNA1 segment was targeted by an endogenous insect microRNA, miR-263a, which decreased the inhibitory effect of the extension sequence on viral promoter activity. Surprisingly, the expression of miR-263a was negatively regulated by RSV infection. This elaborate coordination between terminal variation of the viral genome and endogenous insect microRNAs controls RSV replication in planthopper, thus reflecting a distinct strategy of adaptation of phytoviruses to insect vectors.
url https://doi.org/10.1371/journal.ppat.1009424
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