Grapevine Red Blotch Virus Is Transmitted by the Three-Cornered Alfalfa Hopper in a Circulative, Nonpropagative Mode with Unique Attributes

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.

Epidemiology of Grapevine Red Blotch Disease Progression in Southern Oregon Vineyards

“…Spatial patterns of infected vines within a vineyard suggest spread by insect vectors (Dalton et al 2019). The three-cornered alfalfa hopper (Spissistilus festinus Say) has been reported to vector red blotch virus (Bahder et al 2016a, Flasco et al 2021, and its epidemiological importance in the secondary spread of the virus from infected vines within a vineyard ecosystem has been revealed by Cieniewicz et al (2018).…”

Transmission of Grapevine Red Blotch Virus by Spissistilus festinus [Say, 1830] (Hemiptera: Membracidae) between Free-Living Vines and Vitis vinifera ‘Cabernet Franc’

“…In vineyards where secondary spread is documented, spatiotemporal increase patterns of GRBV-infected vines point to the presence of an aerial hemipteran vector [3,16,[26][27][28][29]. Of the few vector candidates identified in a diseased 'Cabernet franc' vineyard in Napa County in northern California, Spissistilus festinus [Say, 1830] (Hemiptera: Membracidae), the three-cornered alfalfa hopper, proved to be the most likely candidate [3] and was subsequently reported to vector GRBV [30,31]. Other hemipteran vector candidates were recently described in California [32,33].…”

“…The transmission of GRBV by S. festinus is circulative and non-propagative, i.e., GRBV can only be transmitted if the virus transits through the salivary glands of S. festinus following acquisition, but the virus does not replicate in the insect vector [31]. In comparison with other members of the family Geminiviridae, S. festinus-mediated transmission of GRBV has been demonstrated to be comparatively inefficient, with an extended acquisition period (AAP, 10 days) and an extended inoculation access period (IAP, 4 days) on Vvin 'Cabernet franc' (Cf) grapevines [31]. These atypical transmission characteristics reveal a unique relationship between the S. festinus, GRBV, and Vitis species and highlight the need to further our understanding of transmission biology and disease epidemiology.…”

“…In addition to Vvin, rootstock genotypes [2,3], interspecific hybrids [34], and Muscadine grapes [15], GRBV has been found in free-living vines in northern California [26,31,35,36] and southern Oregon [29]. In contrast, the virus was not detected in free-living vines in New York [26].…”

Screening of grapevine red blotch virus in two European ampelographic collections

“…Similar to what has been reported in a Swiss virus grapevine repository (Reynard et al 2017), the absence of field transmission could be explained by the absence of a vector. In North America, the three-cornered alfalfa hopper, Spissistilus festinus, has been reported as a vector of GRBV (Bahder et al 2016a) and transmission occurs in a circulative, nonpropagative mode (Flasco et al 2021). This insect has not been reported to date in Europe.…”