Grapevine red blotch virus is transmitted by the three-cornered alfalfa hopper in a circulative, nonpropagative mode with unique attributes

Authors: FLASCO, MADISON - Cornell University; HOYLE, VICTORIA - Cornell University; CIENIEWICZ, ELIZABETH - Cornell University; ROY, BRANDON - Cornell University; MCLANE, HEATHER - Cornell University; PERRY, KEITH - Cornell University; LOEB, GREGORY - Cornell University; NAULT, BRIAN - Cornell University; Heck, Michelle; FUCHS, MARC - Cornell University

Submitted to: Phytopathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/17/2021
Publication Date: 3/18/2021
Citation: Flasco, M., Hoyle, V., Cieniewicz, E., Roy, B., Mclane, H., Perry, K., Loeb, G., Nault, B., Heck, M.L., Fuchs, M. 2021. Grapevine red blotch virus is transmitted by the three-cornered alfalfa hopper in a circulative, nonpropagative mode with unique attributes. Phytopathology. https://doi.org/10.1094/PHYTO-02-21-0061-R.
DOI: https://doi.org/10.1094/PHYTO-02-21-0061-R

Interpretive Summary: Grapevine red blotch disease was recognized as a new threat to viticulture in the mid to late 2000s in California. Grapevine red blotch virus was identified as the causative agent in diseased vines. The virus causes red and discolored blotches on the leaves, reduces grape quality, wine quality and lowers yield. The virus is spread within a vinyard by a tiny sap-sucking insect called the three-cornered alfalfa hopper. Insects transmit plant viruses in different ways which are defined by the length of time the virus remains associated with the insect. Understanding these details is critical to develop effective disease management strategies. In this research, an ARS researcher collaborated with university partners to test how the three-cornered alfalfa hopper transmits the virus. Grapevine red blotch virus was discovered to circulate throughout the body of the insect prior to transmission to a new host. Extended periods of time were required for virus uptake into the hopper. Different plant species other than grapes had impacts on the ability of the hopper to spread the virus, underscoring the importance of further research on the transmission of this virus in vineyards.

Technical Abstract: The transmission mode of grapevine red blotch virus (GRBV, genus Grablovirus, family Geminiviridae) by Spissistilus festinus, the three-cornered alfalfa hopper, is unknown. By analogy with other members in the family Geminiviridae, we hypothesized circulative, nonpropagative transmission. Time course experiments revealed GRBV in dissected guts, hemolymph and heads with salivary glands following a 5-, 8- and 10-day exposure to infected grapevines, respectively. After a 15-day acquisition on infected grapevines and subsequent transfer on alfalfa, a non-host of GRBV, the virus titer decreased over time in adult insects, as shown by qPCR. Snap bean proved to be a feeding host of S. festinus and a pseudo-systemic host of GRBV following Agrobacterium tumefaciens-mediated delivery of an infectious clone. The virus was efficiently transmitted by S. festinus from infected snap bean plants to excised snap bean trifoliates (90%) or grapevine leaves (100%) but less efficiently from infected grapevine plants to excised grapevine leaves (10%) or snap bean trifoliates (67%). Transmission of GRBV also occurred transstadially but not via seeds. The virus titer was significantly higher in guts and hemolymph relative to heads with salivary glands, and in adults emanating from third compared with first instars that emerged on infected grapevine plants and developed on snap bean trifoliates. This study demonstrated circulative, nonpropagative transmission of GRBV by S. festinus with an extended acquisition access period compared with other viruses in the family Geminiviridae and marked differences in transmission efficiency between grapevine, the natural host, and snap bean, an alternative herbaceous host.