Abstract
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.
Highlights
Arthropod-borne viruses can be maternally transmitted by female insects to their offspring, it is unknown whether male sperm can directly interact with the arbovirus and mediate its paternal transmission
In the eggs laid by the individual V+♀ leafhoppers that mated with nonviruliferous (V−) ♂ leafhoppers, 22% were positive for Rice gall dwarf virus (RGDV) (Fig. 1b), consistent with our earlier observation[24]; in contrast, 73% were RGDV-positive of the eggs produced by V−♀ leafhoppers that mated with V+♂ (Fig. 1b), indicating that paternal transmission is ~ 3.3 times as efficient as maternal transmission, similar to the efficiency of vertical transmission by field-caught leafhoppers (Fig. 1c)
RGDV infection in the weed A. aequalis was never observed in the field during the winter months, though a very low rate of viral infection in A. aequalis occurred under laboratory conditions (Supplementary Table 1)
Summary
Arthropod-borne viruses (arboviruses) can be maternally transmitted by female insects to their offspring, it is unknown whether male sperm can directly interact with the arbovirus and mediate its paternal transmission. We demonstrate that a preferred mode of parental virus transmission has been evolved by hitchhiking with the sperm of male insect vectors without disturbing sperm functioning in a leafhopper-borne plant reovirus. We have shown recently that transovarial transmission of Rice dwarf virus (RDV), a plant reovirus, is mediated by the specific interaction of the viral capsid protein with the outer membrane protein of an obligate symbiotic bacterium of the vector green rice leafhoppers[20]. We report that a high efficiency of sperm-mediated paternal transmission route of RGDV by male R. dorsalis occurs without affecting the fitness of male insects or their offspring, which may play a vital role in long-term maintenance and spread of RGDV in the field
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