Transovarial Transmission of a Plant Virus Is Mediated by Vitellogenin of Its Insect Vector

Most plant viruses are transmitted by hemipteroid insects. Some viruses can be transmitted from female parent to offspring usually through eggs, but the mechanism of this transovarial transmission remains unclear. Rice stripe virus (RSV), a Tenuivirus, transmitted mainly by the small brown planthopp...

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Published in:PLoS pathogens Vol. 10; no. 3; p. e1003949
Main Authors: Huo, Yan, Liu, Wenwen, Zhang, Fujie, Chen, Xiaoying, Li, Li, Liu, Qifei, Zhou, Yijun, Wei, Taiyun, Fang, Rongxiang, Wang, Xifeng
Format: Journal Article
Language:English
Published: United States Public Library of Science 01.03.2014
Public Library of Science (PLoS)
Subjects:
Agriculture
Animals
Biology
Disease transmission
Eggs
Flowers - virology
Fluorescent Antibody Technique
Health aspects
Hemiptera - virology
Host-parasite relationships
Immunoprecipitation
Insect Vectors - metabolism
Insects
Microbiological research
Microscopy
Microscopy, Immunoelectron
Oryza - virology
Parasites
Plant viruses
Real-Time Polymerase Chain Reaction
Tenuivirus - pathogenicity
Two-Hybrid System Techniques
Virus diseases of plants
Viruses
Vitellogenins - metabolism
Yeast
China
Oryza sativa
Two-Hybrid System Techniques
Animals
Immunoprecipitation
Insect Vectors
Fluorescent Antibody Technique
Vitellogenins
Flowers
Tenuivirus
Hemiptera
Real-Time Polymerase Chain Reaction
Microscopy, Immunoelectron
ISSN:1553-7374, 1553-7366, 1553-7374
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Summary:Most plant viruses are transmitted by hemipteroid insects. Some viruses can be transmitted from female parent to offspring usually through eggs, but the mechanism of this transovarial transmission remains unclear. Rice stripe virus (RSV), a Tenuivirus, transmitted mainly by the small brown planthopper (Laodelphax striatellus), is also spread to the offspring through the eggs. Here, we used the RSV-planthopper system as a model to investigate the mechanism of transovarial transmission and demonstrated the central role of vitellogenin (Vg) of L. striatellus in the process of virus transmission into the eggs. Our data showed Vg can bind to pc3 in vivo and in vitro and colocalize in the germarium. RSV filamentous ribonucleoprotein particles (RNPs) only accumulated in the terminal filaments and pedicel areas prior to Vg expression and was not present in the germarium until Vg was expressed, where RSV RNPs and Vg had colocalized. Observations by immunoelectron microscopy (IEM) also indicated that these two proteins colocalized in nurse cells. Knockdown of Vg expression due to RNA interference resulted in inhibition of the invasion of ovarioles by RSV. Together, the data obtained indicated that RSV RNPs may enter the nurse cell of the germarium via endocytosis through binding with Vg. Finally, the virus enters the oocytes through nutritive cords, using the same route as for Vg transport. Our results show that the Vg of L. striatellus played a critical role in transovarial transmission of RSV and shows how viruses can use existing transovarial transportation systems in insect vectors for their own purposes.
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Conceived and designed the experiments: XW RF. Performed the experiments: YH WL FZ XC LL QL YZ TW XW. Analyzed the data: YH WL. Contributed reagents/materials/analysis tools: YZ. Wrote the paper: XW RF TW.
The authors have declared that no competing interests exist.
ISSN:1553-7374
1553-7366
1553-7374
DOI:10.1371/journal.ppat.1003949