Diaphorina citri reovirus (DcRV) was previously identified based on metagenomics surveys for virus discovery. Here, we demonstrated that DcRV induces persistent infections in its psyllid host, Diaphorina citri. DcRV was efficiently vertically passed to offspring in a biparental manner. Transmission electron microscopic and immunological analysis showed that the DcRV-encoded nonstructural protein, P10, assembled into a virion-packaging tubular structure which is associated with the spread of DcRV throughout the bodies of D. citri. P10 tubules containing virions were associated with oocytes of female and sperm of male D. citri, suggesting a role in the highly efficient biparental transmission of DcRV. Knocking down P10 by RNA interference for males reduced the percentage of DcRV-infected progeny, and for females reduced the viral accumulation in progeny. These results, for the first time, show that a nonstructural protein of a novel insect reovirus provides a safe and pivotal channel for virus spread and biparental transmission to progeny.
IMPORTANCE The Asian citrus psyllid, Diaphorina citri Kuwayama, is an important pest in the worldwide citrus industry. It is the vector of Candidatus Liberibacter asiaticus (CLas), the bacterial pathogen of Huanglongbing (HLB), which is currently considered to be the most destructive disease of citrus worldwide. Diaphorina citri reovirus (DcRV) was previously identified based on metagenomics surveys for virus discovery. Here, we found that this novel and persistent insect reovirus took advantage of a viral-encoded nonstructural protein, P10, for efficient vertical transmission from parents to progeny. The P10 assembled into a virion-packaging tubular structure, and was associated with oocytes of female D. citri and sperm of males. Consistently, knockdown of P10 for either male or female D. citri inhibited DcRV transmission to offspring. This tubular strategy for viral spread and biparental transmission might serve as a target for controlling viral vertical transmission and population expansion.