The cultivated grape Vitis vinifera and hybrids of V. vinifera or of other Vitis species (e.g. those used for rootstocks) as well as free-living North American Vitis are the only known natural hosts of GRBV (Perry et al., 2016; Bahder et al., 2016a; Cieniewicz et al., 2017). Due to the significant presence of the red blotch disease in North American vineyards, extensive searches for GRBV natural hosts have been performed there (Krenz et al., 2014). Free-living grapevines found to be infected include hybrids of V. californica × V. vinifera, or hybrids between V. californica and grapevine hybrid rootstocks such as Rugerri 140 and Vitis rupestris St George (Perry et al., 2016; Cieniewicz et al., 2017). Many cultivars of Vitis vinifera have been found to be hosts for GRBV (Krenz et al., 2014; Adiputra et al., 2018) so it should be assumed that most if not all grapevine varieties could be hosts. Blackberry (Rubus armeniacus) has been suggested as an alternative host of GRBV in Northern California, but tests indicated that the virus did not replicate in this host (Bahder et al., 2016a) and this hypothesis has not been confirmed. No herbaceous natural or experimental hosts are known for GRBV (Cieniewicz et al., 2019)

GRBV is widespread in the major grape growing areas of the USA (Al Rwahnih et al., 2013; Krenz et al., 2014) and in some USA germplasm repositories. It is also present in the main grape growing regions of Canada: British Columbia and Ontario (Poojari et al., 2017; Xiao et al., 2018) and in Mexico (Gasperin-Bulbarela et al., 2019). It has also been reported from South America (Luna et al., 2019) and from Asia (Lim et al., 2016; Marwal et al., 2018). A report from Switzerland is related to grapevine material from North America introduced in a germplasm collection. These accessions were removed from the collection and the virus absence was confirmed in this country based on a survey of more than 3,000 grapevines from commercial vineyards (Reynard et al., 2018).

In the absence of surveys, GRBV might be present at low frequency in other regions of the world as its symptoms can easily be confused with those of grapevine leafroll disease, of phytoplasma infections or with symptomatology due to abiotic stress.

As with most other plant viruses, GRBV is graft-transmissible; several epidemiological studies suggest that its wide detection in most of the grape-growing regions of the USA might be correlated with dissemination through GRBV-infected grapevine propagation materials (Sudarshana et al., 2015). In infected grapevines, GRBV gives systemic infections and spreads widely within the infected plants.

As with many other members of the Geminiviridae family, GRBV is assumed to be phloem-limited (Sudarshana et al., 2015), suggesting that phloem-feeding vectors might be involved in its horizontal spread. Indeed, spread from red blotch-infected vineyards to neighbouring healthy plots, as well as clustering of infected vines strongly suggested that an aerial vector was involved in GRBV transmission. In a greenhouse study the three-cornered alfalfa hopper (3CAH), Spissistilus festinus (Say) (Hemiptera: Membracidae) has been experimentally shown to transmit GRBV (Bahder et al., 2016b). Recent results suggest that this transmission is in a circulative, non-propagative mode (Flasco et al., 2021). In California, the highest population density and ratio of viruliferous S. festinus were identified in June and July (Cieniewicz et al., 2018a); a recent epidemiological study revealed an annual spread of 1 to 2% of GRBV in a Californian vineyard (Cieniewicz et al., 2018b). Although S. festinus is polyphagous and can feed on vine, it has not been reported to reproduce on grapevine (Preto et al., 2018). Nevertheless, this treehopper can feed and reproduce on a variety of plant species found in and around vineyards, including some cover crops and weeds [Vicia benghalensis (purple vetch), Trifolium alexandrinum (berseem clover), Lolium multiflorum (annual ryegrass), Fagopyrum esculentum (buckwheat), Triticum x Secale (triticale), Vulpia myuros (Zorro fescue)]. The legume species (purple vetch and berseem clover) exhibited higher nymph emergence (Kron and Sisterson, 2020). In addition to S. festinus, GRBV has been detected by multiplex PCR in other phloem-sucking insects: Colladonus reductus (Cicadellidae), Osbornellus borealis (Cicadellidae) and Melanoliarus sp. (Cixiidae) but there is to date no proof that these other species might be able to transmit GRBV (Cieniewicz et al., 2018b). A recent unpublished report suggests that the ragweed treehopper (Entylia carinata) and the two-marked treehopper (Enchenopa binotata) might be able to transmit GRBV (Smith et al., 2020).

In addition, vineyard observations validated the hypothesis of an association between GRBV spread dynamics and abundance of S. festinus populations (Cieniewicz et al., 2019), demonstrating the epidemiological relevance of this Membracidae.

Symptoms

Symptoms occur on leaves and berries. They appear on the older leaves of the canopy between spring and summer, and migrate to the upper part of the plants at the end of summer or, beginning of autumn. For red-berried varieties, red blotches are visible on leaves early in the growing season, and can then coalesce during summer with variations in the red colour. On white-berried varieties, leaf symptoms consist of chlorotic spots, that can eventually evolve into necrotic lesions (Sudarshana et al., 2015; Cieniewicz et al., 2017). Accumulation of anthocyanins in leaves precedes other signs of senescence. On berries, besides impact on yield, a delay and heterogeneity in ripening are seen and fruit juice quality and anthocyanin accumulation are negatively affected through a hypothesized disruption in hormone signalling (Blanco-Ulate et al., 2017). Anthocyanin concentration was generally reduced in GRBV positive vines, by between 18% and 30% with yearly variations in Pinot Noir (Levin and Achala, 2020). Total soluble solids are also reduced at harvest, and berries of red varieties exhibited reduced polyphenolic content (Girardello et al., 2019; Martinez-Luscher et al., 2019).

The similarities in symptoms on leaves and fruits between GRBD and grapevine leafroll disease are the most probable reason that red blotch disease took such a long time to be recognized. Grapevine leafroll-associated virus-3, which is regarded as the most important causal agent of grapevine leafroll disease, another phloem-limited virus, is thought to act via similar mechanisms which could explain the similarities in symptomology (Martinez-Luscher et al., 2019). Symptom confusion on red-berried cultivars could also be made with those resulting from Pierce’s disease, and with arthropod damage as well as abiotic stresses such as nutrient deficiencies (magnesium and chloride) (Cieniewicz et al., 2017).

Morphology

GRBV virions visualization through electron microscopy has never been clearly documented, whether from crude sap homogenates or from attempts at particle purification. Nevertheless, being classified as a gemini-like virus, GRBV virions would be expected to be geminate, consisting of twined icosahedra of approximately 22 x 38 nm with a sedimentation coefficient of about 70S. GRBV has a monopartite genome consisting of a single-stranded circular DNA molecule of approximately 3.2 kilobases, encoding 6 partly overlapping open reading frames (ORFs). The gene expression strategy is similar to that seen in other of the Geminiviridae family members (Cieniewicz et al., 2017; Vargas-Asencio et al., 2019). The genome encodes 3 ORFs in the virion sense; V1 (CP of 25.3 kDa), V2 and V3 (hypothesized to be movement proteins). There are also 3 ORFs in the complementary sense, C1, C2 and C3. As Geminiviridae do not encode a functional DNA polymerase, replication is performed by recruitment of host factors enabling the viral DNA synthesis. The splicing of the complementary sense transcript produces a replication-associated protein (Rep), that is essential for virus ssDNA synthesis.

Detection and inspection methods

A procedure for inspection of places of production of Vitis plants for planting is provided in Standard PM 3/85 (EPPO, 2018). Given the possible confusion with leafroll disease foliar symptoms, in particular in red-berried varieties, symptoms are not sufficiently reliable to establish the presence of GRBV in a vineyard. Moreover, it has not yet been possible to isolate viral particles from GRBV-infected plants, thereby hampering the development of serological reagents and assays that would facilitate GRBV detection using serological procedures such as ELISA. Nucleic acids-based methods are therefore the only available options for GRBV detection. PCR and real-time PCR multiplex tests have been developed with primers covering the genetic diversity of GRBV (Krenz et al., 2014) and used in mother plants blocks, nurseries and vineyards. Spatiotemporal fluctuations in GRBV detection leading to erratic detection results during some periods of the year have been reported using PCR or real-time PCR. A recent well-documented methodological study (Setiono et al., 2018), using an optimized real-time PCR, has proposed a useful guide for the reliable and sensitive detection of GRBV in field-grown grapevines, highlighting the variability of virus distribution in the vine and identifying the best sampling period. The study found that petioles of older leaves are the richest source of GRBV, while emerging leaves exhibit the lowest viral DNA content, similar to that which has been extensively reported for grapevine leafroll-associated viruses using ELISA assays. In the USA, the best period of sampling was shown to be between July and October, the virus reaching a ‘saturation’ titre at the end of the growing season (Setonio et al., 2018).

Mass spectrometry has also been applied to quantify GRBV in infected plants and identify potential biomarkers of viral infection, by detecting two GRBV proteins (coat protein and V2 protein) in tissue lysates (Buchs et al., 2018). Finally, as an alternative to more classical methods, a novel plasmonic CRISPR Cas12a assay has also been recently proposed with successful detection of GRBV from grapevine samples from commercial vineyards, generating a colorimetric signal that can be exploited under field conditions without the need for bench instruments for readout (Li et al., 2019).

Given the efficient transmission of GRBV through vegetative propagation practices, the main pathway for long-distance movement is the circulation and trade of infected grapevine propagation materials. A minor entry pathway could be through the movement of viruliferous Spissistilus festinus vectors, on their own or hitchhiking on plants other than Vitis. In countries where it is present, the vector represents the main means of local spread of the virus.

Economic impact

GRBV infection has been shown to affect many aspects of vine physiology from leaf metabolism (Wallis and Sudarshana, 2016) to fruit development and ripening (Blanco-Ulate et al., 2017). Economic losses can be severe and are a consequence of a reduction in fruit and wine quality as well as reductions in vegetative growth and canopy development. The economic impact has been estimated in the grape-growing regions in the United States, on Cabernet-Sauvignon in California and on Merlot in Washington State and New York, reaching between 2 200 - 68 500 USD per hectare over a 25-year production period (Ricketts et al., 2017). This is similar to the losses that have been estimated for the leafroll disease. However, while GRBV infection may not cause long-term productivity decline if vines are infected once mature, it remains unclear to what degree management practices post-infection and/or vine age at time of infection may influence the outcome (Levin and Achala, 2020).

Control

There is no curative treatment available to control the red blotch disease in vineyards, so all control strategies are based on prophylaxis or on control of insect vectors. In this context, a key control element is the use of GRBV-free planting materials (Cieniewicz et al., 2017). Thus, implementation of GRBV testing worldwide in certification and quarantine programs to prevent the spread of this virus are well established or should be considered.

In US vineyards, Ricketts et al. (2017) suggested that roguing symptomatic vines and replanting with clean vines derived from GRBV-free stocks would minimize losses if GRBD incidence is low to moderate (below 30%), while a full vineyard replacement should be pursued if disease incidence is higher. Another economic study aiming at mitigating red blotch disease showed that in a 10 year-old Pinot Noir vineyard there were no significant effects of water deficits on foliar symptoms onset, but there was a more rapid progression of symptoms in a year with more severe water deficits (Levin and Achala, 2020). Although keeping GRBV positive vines well-watered may mitigate some of the negative effects of GRBD, this study also suggested that watering management may not improve overall fruit quality in GRBV infected vines (Levin and Achala, 2020).

The role of infected free-living vines as alternate hosts and GRBV reservoirs requires further investigation (Cieniewicz et al., 2018b). Indeed, the directionality of GRBV spread between cultivated grapevines and wild Vitis remains an open question and a better understanding of the epidemiology of GRBV will be essential for the development of more efficient control strategies. In any case, the possibility of the existence of a reservoir in wild grapevines should not be dismissed in any eradication efforts (Cieniewicz et al., 2018a; Cieniewicz et al., 2018b).

Systematic control of the insect vector, Spissistilus festinus, using insecticides is currently not recommended (Cieniewicz et al., 2019), but may complement other management strategies once the phenology of this insect and its efficiency as a vector are better understood (Cieniewicz et al., 2017).

Phytosanitary risk

The phytosanitary risk is essentially linked to infected grapevine propagation material and seen as significant for the whole EPPO Vitis production area given the clear pathogenicity and potential for negative impact of GRBV. In the EPPO region, the risk is mitigated by the absence of the Spissistilus festinus vector but the possibility exists that some European species such as Stictocephala bisonia (Membracidae) might be able to transmit GRBV. EFSA (2019) considered that, except for those affecting the host, no eco-climatic constraints exist for GRBV. Therefore, it is expected that GRBV is able to establish wherever Vitis are cultivated, causing symptoms and having impacts on Vitis fruit yield and/or quality.

As drafted in an EPPO PRA Report (EPPO, in preparation) based on the EFSA pest categorization (EFSA, 2019), appropriate phytosanitary measures to import Vitis plants for planting (other than seeds) into the EPPO region could require that these plants are produced in a pest free area or in a pest free place/site of production for GRBV established according to EPPO Standard PM 5/8 Guidelines on the phytosanitary measure ‘Plants grown under physical isolation’ (EPPO, 2016). The physical isolation should allow to prevent both the virus and the vector from entering the place/site of production. A system approach combining the absence of GRBV symptoms during the growing period, testing of the consignment for GRBV and treatment of the consignment for the vector can also be envisaged. A number of EPPO countries already ban the import of Vitis plants for planting (other than seeds) (e.g. EU countries: Annex VI, points 10 of Regulation 2019/2072 (EU, 2019)). Host plants for planting could also be imported using post-entry quarantine (in the framework of a bilateral agreement).

Adiputra J, Kesoju SR & Naidu RA (2018) The relative occurrence of Grapevine leafroll-associated virus 3 and Grapevine red blotch virus in Washington State vineyards. Plant Disease 102, 2129-2135.

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Al Rwahnih M, Dave A, Anderson M, Rowhani A, Uyemoto J & Sudarshana M, (2013) Association of a DNA virus with grapevines affected by red blotch disease in California. Phytopathology 103, 1069-1076.

Al Rwahnih M, Rowhani A & Golino D (2015a) First report of Grapevine red blotch-associated virus in archival grapevine material from Sonoma County, California. Plant Disease 99, 895-895.

Al Rwahnih M, Rowhani A, Golino D, Islas C, Preece J & Sudarshana M (2015b) Detection and genetic diversity of Grapevine red blotch-associated virus isolates in table grape accessions in the National Clonal Germplasm Repository in California. Canadian Journal of Plant Pathology 37, 130-135.

Bahder BW, Zalom FG & Sudarshana MR (2016a) An evaluation of the flora adjacent to wine grape vineyards for the presence of alternative host plants of Grapevine red blotch-associated virus. Plant Disease 100, 1571-1574.

Bahder BW, Zalom FG, Jayanth M & Sudarshana MR (2016b) Phylogeny of Geminivirus coat protein sequences and digital PCR aid in identifying Spissistilus festinus as a vector of Grapevine red blotch-associated virus. Phytopathology 106, 1223-1230.

Blanco-Ulate B, Hopfer H, Figueroa-Balderas R, Ye Z, Rivero RM, Albacete A, Perez-Alfocea F, Koyama R, Anderson MM, Smith RJ, Ebeler SE & Cantu D (2017) Red blotch disease alters grape berry development and metabolism by interfering with the transcriptional and hormonal regulation of ripening. Journal of Experimental Botany 68, 1225-1238.

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EPPO (2016) EPPO Standard PM 5/8 Guidelines on the phytosanitary measure ‘Plants grown under complete physical isolation’. EPPO Bulletin 46, 421-423. Available at https://gd.eppo.int/standards/PM5/ 

EPPO (in preparation) Report of a pest risk analysis for grapevine red blotch virus. EPPO, Paris. Available soon at https://gd.eppo.int/taxon/GRBAV0/documents

EU (2019) Commission implementing regulation 2019/2072 of 28 November 2019 establishing uniform conditions for the implementation of Regulation (EU) 2016/2031 of the European Parliament and the Council, as regards protective measures against pests of plants, and repealing Commission Regulation (EC) No 690/2008 and amending Commission Implementing Regulation (EU) 2018/2019. Version of 2019-12-10. Official Journal of the European Union L319, 1-278.

Flasco M, Hoyle V, Cieniewicz EJ, Roy B, McLane H, Perry KL, Loeb GM, Nault B, Cilia M & Fuchs M (2021) Grapevine red blotch virus is transmitted by the three-cornered alfalfa hopper in a circulative, nonpropagative mode with unique attributes. Phytopathology, online first, https://doi.org/10.1094/PHYTO-02-21-0061-R

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Gasperin-Bulbarela J, Licea-Navarro AF, Pino-Villar C, Hernandez-Martinez R & Carrillo-Tripp J (2019) First report of Grapevine red blotch virus in Mexico. Plant Disease 103, 381-381.

Girardello RC, Cooper ML, Smith RJ, Lerno LA, Bruce RC, Eridon S & Oberholster A (2019) Impact of Grapevine red blotch disease on grape composition of Vitis vinifera Cabernet Sauvignon, Merlot, and Chardonnay. Journal of Agricultural and Food Chemistry 67, 5496-5511.

Krenz B, Thompson JR, McLane HL, Fuchs M & Perry KL (2014) Grapevine red blotch-associated virus is widespread in the United States. Phytopathology 104, 1232-1240.

Kron CR & Sisterson MS (2020) Identification of nonhost cover crops of the three-cornered alfalfa hopper (Spissistilus festinus). American Journal of Enology and Viticulture 71, 175-180.

Levin AD & Achala NKC (2020) Water deficits do not improve fruit quality in Grapevine red blotch virus-infected grapevines (Vitis vinifera L.). Frontiers in Plant Science 11, 1292.

Li Y, Mansour H, Wang T, Poojari S & Li F (2019) Naked-eye detection of Grapevine red-blotch viral infection using a plasmonic CRISPR Cas12a assay. Analytical Chemistry 91, 11510-11513.

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Martinez-Luscher J, Plank CM, Brillante L, Cooper ML, Smith RJ, Al-Rwahnih M, Yu R, Oberholster A, Girardello R & Kurtural SK (2019) Grapevine red blotch virus may reduce carbon translocation leading to impaired grape berry ripening. Journal of Agricultural and Food Chemistry 67, 2437-2448.

Marwal A, Kumar R, Verma RK, Mishra M & Gaur RK (2018) Complete nucleotide sequence of a DNA virus isolated from Vitis vinifera in India: A symptomless host of Grapevine red blotch virus. Virus Disease 30, 106-111.

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Perry KL, McLane H, Hyder MZ, Dangl GS, Thompson JR & Fuchs MF (2016) Grapevine red blotch-associated virus is present in free-living Vitis spp. proximal to cultivated grapevines. Phytopathology 106, 663-670.

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Poojari S, Lowery DT, Rott M, Schmidt AM & Urbez-Torres JR (2017) Incidence, distribution and genetic diversity of Grapevine red blotch virus in British Columbia. Canadian Journal of Plant Pathology 39, 201-211.

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Ricketts KD, Gomez MI, Fuchs MF, Martinson TE, Smith RJ, Cooper ML, Moyer MM & Wise A (2017) Mitigating the economic impact of grapevine red blotch: optimizing disease management strategies in US vineyards. American Journal of Enology and Viticulture 68, 127-135.

Setiono FJ, Chatterjee D, Fuchs M, Perry KL & Thompson JR (2018) The distribution and detection of Grapevine red blotch virus in its host depend on time of sampling and tissue type. Plant Disease 102, 2187-2193.

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Wallis CM & Sudarshana MR (2016) Effects of Grapevine red blotch-associated virus (GRBaV) infection on foliar metabolism of grapevines. Canadian Journal of Plant Pathology 38, 358-366.

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This datasheet was prepared in 2021 by Drs Olivier Lemaire and Thierry Candresse. Their valuable contribution is gratefully acknowledged.

This datasheet was first published online in 2021. It is maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.