Submitted to: Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/11/2021
Publication Date: 7/13/2021
Citation: Stenger, D.C., Krugner, R. 2021. Insect-to-insect horizontal transmission of a phytoreovirus in the absence of an infected plant host. Virology. 562:87-91. https://doi.org/10.1016/j.virol.2021.07.006.
Interpretive Summary: Phytoreoviruses are double-stranded RNA viruses which typically systemically infect both plant hosts and insect vectors. Direct transmission of phytoreoviruses among vector insects is reported to be vertical (mother to progeny, transovarily). Horizontal transmission from insect to insect is indirect, with vector insects inoculating host plants that subsequently become systemically infected and which may serve as a source of virus to infect naive vector insects. Homalodisca vitripennis reovirus (HoVRV) is an atypical phytoreovirus known only to infect an insect (glassy-winged sharpshooter); no plant host is known. HoVRVoccurs in high incidence (90-100%) in glassy-winged sharpshooter populations residing in citrus orchards of Southern California, despite citrus being immune to HoVRV. These oddities prompted experiments to determine mode (vertical versus horizontal) of insect-to-insect transmission of HoVRV in glassy-winged sharpshooter. Vertical transmission assays revealed HoVRV was transmitted transovarily from mother to progeny at low frequency (6%), a level insufficient to explain near universal incidence of HoVRV in field populations. Two routes of insect-to-insect horizontal transmission of HoVRV were investigated. Indirect insect-to-insect horizontal transmission (via passive movement of virions through the xylem of immune citrus seedlings) was tested by placing infected adult source insects in one cage and uninfected naive test insects in another cage on the same plant. No indirect horizontal transmission of HoVRV was observed. In contrast, when HoVRV infected adults were placed in the same cage as naive, uninfected test insects (nymphs so they could be distinguished from source insects), direct insect-to-insect horizontal transmission was observed at frequencies up to 33% after an exposure period of 7 days. Collectively, low frequency of vertical transmission coupled with more efficient direct horizontal transmission reasonably explains high incidence of HoVRV in dense glassy-winged sharpshooter populations. Further, these data and conclusions suggest that routes of insect-to-insect transmission of other phytoreoviruses (some of which are significant economic pests of rice) should be re-evaluated.
Technical Abstract: Vertical transmission of Homalodisca vitripennis reovirus (HoVRV) from glassy-winged sharpshooter (GWSS, Homalodisca vitripennis Germar) females to progeny occurred in laboratory assays at rates too low (2.6% to 15.4%) to account for HoVRV incidence (90 – 100%) in field populations resident in citrus. As citrus is immune to HoVRV and no plant host is known, horizontal transmission of HoVRV from insect-to-insect was evaluated. Exposure of colony-reared virus-free test nymphs to HoVRV-infected source adults held in the same cage for two weeks on virus-immune cowpea resulted in HoVRV transmission (13.3% to 30.7%) to test nymphs. HoVRV was not transmitted when exposure was indirect and required passive movement of HoVRV virions through the xylem of immune citrus seedlings. Collectively, these results demonstrate direct insect-to-insect horizontal transmission of HoVRV, providing a plausible explanation for high incidence of HoVRV in GWSS field populations in the absence of efficient vertical transmission. We further suggest that re-evaluation of insect-to-insect transmission of other plant-infecting reoviruses (species of Phytoreovirus, Fijivirus, and Orthoreovirus reported to be efficiently transmitted vertically from insect to insect) be re-assessed in similar experiments that clearly distinguish horizontal from vertical transmission.