A Nonstructural Protein Responsible for Viral Spread of a Novel Insect Reovirus Provides a Safe Channel for Biparental Virus Transmission to Progeny

Qian Chen; Kris Godfrey; Jiejie Liu; Qianzhuo Mao; Yen-Wen Kuo; Bryce W Falk

doi:10.1128/JVI.00702-19

A Nonstructural Protein Responsible for Viral Spread of a Novel Insect Reovirus Provides a Safe Channel for Biparental Virus Transmission to Progeny

J Virol. 2019 Jul 17;93(15):e00702-19. doi: 10.1128/JVI.00702-19. Print 2019 Aug 1.

Authors

Qian Chen^{1

2}, Kris Godfrey³, Jiejie Liu², Qianzhuo Mao², Yen-Wen Kuo¹, Bryce W Falk⁴

Affiliations

¹ Department of Plant Pathology, University of California, Davis, California, USA.
² Fujian Province Key Laboratory of Plant Virology, Institute of Plant Virology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, People's Republic of China.
³ Contained Research Facility, University of California, Davis, California, USA.
⁴ Department of Plant Pathology, University of California, Davis, California, USA bwfalk@ucdavis.edu.

Abstract

Diaphorina citri reovirus (DcRV) was previously identified based on metagenomics surveys for virus discovery. Here, we demonstrated that DcRV induces persistent infection in its psyllid host, Diaphorina citri DcRV was efficiently vertically passed to offspring in a biparental manner. Transmission electron microscopic and immunological analyses 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 insects. P10 tubules containing virions were associated with oocytes of female and sperm of male D. citri insects, 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," the bacterial pathogen of Huanglongbing, which is currently considered the most destructive disease of citrus worldwide. 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 virus-encoded nonstructural protein, P10, for efficient vertical transmission from parents to progeny. P10 assembled into a virion-packaging tubular structure and was associated with oocytes of female D. citri and sperm of males. Consistent with this, knockdown of P10 for either male or female D. citri insects 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.

Keywords: Diaphorina citri; Diaphorina citri reovirus; biparental transmission; insect reovirus; sperm; transovarial transmission; tubule.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animal Structures / virology
Animals
Hemiptera / virology*
Infectious Disease Transmission, Vertical*
Male
Oocytes / virology
Protein Multimerization*
Reoviridae / isolation & purification*
Reoviridae Infections / transmission
Reoviridae Infections / veterinary*
Spermatozoa / virology
Viral Nonstructural Proteins / metabolism*

Substances

Viral Nonstructural Proteins