Viral pathogens hitchhike with insect sperm for paternal transmission

Arthropod-borne viruses (arboviruses) can be maternally transmitted by female insects to their offspring, however, it is unknown whether male sperm can directly interact with the arbovirus and mediate its paternal transmission. Here we report that an important rice arbovirus is paternally transmitte...

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Bibliographic Details
Published in:Nature communications Vol. 10; no. 1; pp. 955 - 10
Main Authors: Mao, Qianzhuo, Wu, Wei, Liao, Zhenfeng, Li, Jiajia, Jia, Dongsheng, Zhang, Xiaofeng, Chen, Qian, Chen, Hongyan, Wei, Jing, Wei, Taiyun
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 27.02.2019
Nature Publishing Group
Nature Portfolio
Subjects:
13/1
13/89
14/19
14/28
38/77
45/23
45/90
631/326/421
631/326/596
82/58
82/80
82/83
Amino Acid Sequence
Animals
Arboviruses - pathogenicity
Capsid protein
Disease transmission
Epidemics
Female
Fitness
Hemiptera - genetics
Hemiptera - virology
Heparan sulfate
Host Microbial Interactions - genetics
Host Microbial Interactions - physiology
Humanities and Social Sciences
Insect Proteins - genetics
Insect Proteins - physiology
Insect Vectors - genetics
Insect Vectors - virology
Insects
Male
multidisciplinary
Offspring
Oryza
Oryza - virology
Plant Diseases - virology
Plant Viruses - pathogenicity
Proteins
Proteoglycans
Reoviridae - pathogenicity
Reoviridae - physiology
Science
Science (multidisciplinary)
Sequence Homology, Amino Acid
Sperm
Spermatozoa - ultrastructure
Spermatozoa - virology
Sulfates
Viruses
ISSN:2041-1723, 2041-1723
Online Access:Get full text
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Summary:Arthropod-borne viruses (arboviruses) can be maternally transmitted by female insects to their offspring, however, it is unknown whether male sperm can directly interact with the arbovirus and mediate its paternal transmission. Here we report that an important rice arbovirus is paternally transmitted by the male leafhoppers by hitchhiking with the sperm. The virus-sperm binding is mediated by the interaction of viral capsid protein and heparan sulfate proteoglycan on the sperm head surfaces. Mating experiments reveal that paternal virus transmission is more efficient than maternal transmission. Such paternal virus transmission scarcely affects the fitness of adult males or their offspring, and plays a pivotal role in maintenance of viral population during seasons unfavorable for rice hosts in the field. Our findings reveal that a preferred mode of vertical arbovirus transmission has been evolved by hitchhiking with insect sperm without disturbing sperm functioning, facilitating the long-term viral epidemic and persistence in nature. Arbovirus vertical transmission is commonly mediated by transovarial passage of female insect vectors. Here, the authors show that Rice gall dwarf virus can be transmitted by male leafhoppers via interactions of the viral capsid and heparan sulfate proteoglycan on the surface of sperm heads.
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ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-019-08860-4