F-actin dynamics in midgut cells enables virus persistence in vector insects.


Journal

Molecular plant pathology
ISSN: 1364-3703
Titre abrégé: Mol Plant Pathol
Pays: England
ID NLM: 100954969

Informations de publication

Date de publication:
11 2022
Historique:
revised: 29 06 2022
received: 25 04 2022
accepted: 06 07 2022
pubmed: 9 9 2022
medline: 18 10 2022
entrez: 8 9 2022
Statut: ppublish

Résumé

Hemipteran insects that transmit plant viruses in a persistent circulative manner acquire, retain and transmit viruses for their entire life. The mechanism enabling this persistence has remained unclear for many years. Here, we determined how wheat dwarf virus (WDV) persists in its leafhopper vector Psammotettix alienus. We found that WDV caused the up-regulation of actin-depolymerizing factor (ADF) at the mRNA and protein levels in the midgut cells of leafhoppers after experiencing a WDV acquisition access period (AAP) of 6, 12 or 24 h. Experimental inhibition of F-actin depolymerization by jasplakinolide and dsRNA injection led to lower virus accumulation levels and transmission efficiencies, suggesting that depolymerization of F-actin regulated by ADF is essential for WDV invasion of midgut cells. Exogenous viral capsid protein (CP) inhibited ADF depolymerization of actin filaments in vitro and in Spodoptera frugiperda 9 (Sf9) cells because the CP competed with actin to bind ADF and then blocked actin filament disassembly. Interestingly, virions colocalized with ADF after a 24-h AAP, just as actin polymerization occurred, indicating that the binding of CP with ADF affects the ability of ADF to depolymerize F-actin, inhibiting WDV entry. Similarly, the luteovirus barley yellow dwarf virus also induced F-actin depolymerization and then polymerization in the gut cells of its vector Schizaphis graminum. Thus, F-actin dynamics are altered by nonpropagative viruses in midgut cells to enable virus persistence in vector insects.

Identifiants

pubmed: 36073369
doi: 10.1111/mpp.13260
pmc: PMC9562576
doi:

Substances chimiques

Actins 0
Capsid Proteins 0
RNA, Messenger 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1671-1685

Informations de copyright

© 2022 The Authors. Molecular Plant Pathology published by British Society for Plant Pathology and John Wiley & Sons Ltd.

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Auteurs

Hui Wang (H)

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.
State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fuzhou, China.

Yan Liu (Y)

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.

Wenwen Liu (W)

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.

Kongming Wu (K)

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.

Xifeng Wang (X)

State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China.

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Classifications MeSH