Comparative Performance of Virus-Infected Vitis vinifera cv. Savagnin rose Grafted onto Three Rootstocks
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1 Comparative Performance of Virus-Infected Vitis vinifera cv. Savagnin rose Grafted onto Three Rootstocks Véronique Komar, 1 Emmanuelle Vigne, 1 Gérard Demangeat, 1 Olivier Lemaire, 1 and Marc Fuchs 2 * Abstract: The combined effect of infection status of three Vitis vinifera cv. Savagnin rose clones and rootstock on vigor, yield, and fruit quality was determined in a replicated field trial from 1999 to Savagnin clone 511 was infected with Grapevine leafroll-associated virus 1 (GLRaV-1), Grapevine virus A (GVA), Rupestris stem pitting-associated virus (RSPaV), vein mosaic, and vein necrosis (virus combination 1); clone 511A was infected with RSPaV, vein mosaic, and vein necrosis (virus combination 2); and clone 511B was healthy. Overall, no significant interaction between infection status and rootstock genotype (Vitis rupestris, Kober 5BB, or Couderc) on the viticultural performance of the three Savagnin rose clones was observed. These findings imply that there is no association between the vegetative and productive performance of scion material infected with virus combination 1 or 2 and susceptibility of Kober 5BB, V. rupestris, and Couderc to the Kober stem-grooving and rupestris stem-pitting syndromes, respectively. Nonetheless, virus combination 1 significantly reduced vigor (19 to 23%) and yield (42 to 54%) over six consecutive years, while virus combination 2 had no major impact on growth and production. Neither virus combination significantly affected soluble sugars or titratable acidity of fruit juice. Key words: grape, virus and viruslike diseases, rootstock, viticultural performance Graft-transmissible viruses associated with leafroll and rugose wood diseases are prevalent and widespread in grapevines. Ten distinct virus species are associated with leafroll (Abou Ghanem-Sabanadzovic et al. 2006, Martelli 2006), while rugose wood is a disease complex consisting of four syndromes: corky bark (CB), LN33 stem-grooving, rupestris stem-pitting (RSP), and Kober stem-grooving (KSG) (Martelli 2006, Martelli and Boudon-Padieu 2006, Rowhani et al. 2005). The rootstocks Kober 5BB (Vitis berlandieri x V. riparia) and V. rupestris du Lot serve as specific biological indicators for KSG and RSP, respectively (Martelli and Boudon-Padieu 2006, Rowhani et al. 2005). The etiology of the rugose wood disease complex is not fully resolved, although Grapevine virus A (GVA) and Grapevine virus B are closely associated with KSG and CB, 1 Institut National de la Recherche Agronomique and Université de Strasbourg, UMR 1131, Unité Mixte de Recherche Santé de la Vigne et Qualité du Vin, BP 20507, Colmar, France; and 2 Department of Plant Pathology and Plant- Microbe Biology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY *Corresponding author ( mf13@cornell.edu; tel: ; fax: ) Acknowledgments: The authors are grateful to Dennis Gonsalves for providing antiserum to RSPaV, J. Barnard for advice with statistical analyses, L.M. Yepes for critically reading the manuscript, and Paul Bass and René Legin for producing plant material and performing graft indexing. The authors thank Peggy Andret-Link, Marlène Henry, Marie-Louise Bechler, Anne-Marie Chanel, and Daniela Dancea for assistance at harvest. Manuscript submitted June 2009, revised Sept 2009, accepted Nov Publication costs of this article defrayed in part by page fees. Copyright 2010 by the American Society for Enology and Viticulture. All rights reserved. respectively (Martelli and Boudon-Padieu 2006, Rowhani et al. 2005) and there is good correlation between Rupestris stem pitting-associated virus (RSPaV) and RSP (Martelli and Boudon-Padieu 2006, Rowhani et al. 2005). However, Koch s postulates have not been fulfilled for leafroll and rugose wood diseases (Martelli and Boudon-Padieu 2006, Rowhani et al. 2005). Leafroll and rugose wood can detrimentally impact vigor, yield, and fruit quality (Credi et al. 1991, Credi and Babini 1996, Komar et al. 2007, Mannini 2003), although their effect varies with such factors as rootstock genotype, scion cultivar, virus strain, timing of infection, and environmental conditions (Mannini 2003). This means that a virus latent in one grapevine scion cultivar may cause severe symptoms if grafted onto a different rootstock genotype (Golino 1993). Such is the case for scion material infected with Grapevine leafroll-associated virus 2 (GLRaV-2) strain Red Globe, which exhibits a severe decline when grafted onto some rootstocks (Kober 5BB, 1103 Paulsen, 3309 Couderc, 1616 Couderc, and Teleki 5C) (Greif et al. 1995, Golino 2003, Golino et al. 2000, 2003, Uyemoto and Rowhani 2003) but not others (SO4, 110 Richter, Freedom, Harmony, 420A, and Mtg) (Borgo et al. 2006, Komar et al. 2007, Uyemoto and Rowhani 2003). Amid this detrimental interaction between GLRaV-2 strain Red Globe and the above rootstocks, limited information is available on the viticultural performance of virus-infected scion material grafted onto different rootstocks. For example, our knowledge of how GVA and RSPaV influence the vegetative and productive potential of scion material grafted onto Kober 5BB and V. rupestris du Lot is limited. This study determined the viticultural performance of three clones of 68
2 Combined Effect of Rootstock and Virus on Vine Performance 69 V. vinifera cv. Savagnin rose, one healthy and two infected by combinations of viruses and viruslike diseases, grafted onto three rootstock genotypes: Vitis rupestris, Kober 5BB (V. berlandieri x V. riparia), and Couderc (161-49C) (V. riparia x V. berlandieri). Materials and Methods Plant material. Vitis vinifera cv. Savagnin rose was used in this study. Savagnin rose is a less aromatic form of V. vinifera cv. Gewürztraminer, which is commonly referred to as Klevener de Heiligenstein in the Alsace region of France. Clone 511 of Savagnin rose was from a commercial vineyard. It was infected with viruses and viruslike diseases (Table 1). Budwood from clone 511 and some of its progeny obtained after virus elimination therapy were grafted onto the certified rootstocks Kober 5BB clone 259, C clone 170, and Vitis rupestris clone 750 for the purpose of this study. Virus elimination. Rooted cuttings of V. vinifera cv. Savagnin rose clone 511 were subjected to virus elimination as described previously (Komar et al. 2007). Briefly, apices from heat-treated plants were grafted onto fragments of hypocotyls from rootstock seedlings (Bass and Vuittenez 1977). Plantlets derived from actively growing apices were propagated in tissue culture and established subsequently in the greenhouse. Graft indexing and double antibody sandwich (DAS) enzyme-linked immunosorbent assay (ELISA) were used to test for the presence of viruslike diseases and viruses, respectively, before and after virus elimination as described (Komar et al. 2007). Graft indexing. Viruses and viruslike diseases were assessed by green-graft indexing in the greenhouse (Walter et al. 1990) using the following indicators: V. vinifera cv. Pinot noir for leafroll, V. rupestris du Lot for rupestris stem-pitting (RSP), Kober 5BB for Kober stem-grooving (KSG), LN33 (1613 Couderc x Thompson Seedless) for corky bark (CB), V. riparia Gloire de Montpellier for fleck and vein mosaic (VM), and 110 Richter (V. rupestris x V. berlandieri) for vein necrosis (VN). DAS-ELISA. DAS-ELISA was carried out with plant crude extracts from leaves (Komar et al. 2007, Walter and Etienne 1987). Antibodies to Grapevine leafroll-associated virus 1 (GLRaV-1) and GVA were produced at INRA- Colmar and antibodies to RSPaV were provided by Dennis Gonsalves, Cornell University. Biotinylated, alkaline phosphatase-tagged conjugates were prepared and used in DAS-ELISA for GLRaV-1, GVA, and RSPaV to enhance the reaction signal, as described (Zimmermann et al. 1990). Substrate hydrolysis was recorded at 405 nm with a Titertek Multiscan MCC/340 reader (Labsystems, Les Ulis, France). Samples were considered positive if their OD 405nm readings were at least twice those of healthy controls. Serological tests were performed with different accessions from the European virus reference collection at INRA-Colmar, France (Greif and Walter 1997) as positive and negative checks. Field trial and experimental approach. An area of homogeneous topographic and soil condition was selected for the field trial on the Huben farm at INRA-Colmar, France. One hundred and fifty vines were planted for V. vinifera cv. Savagnon rose clone 511 and its progeny obtained after virus elimination by heat therapy (clones 511A and 511B), making a total of 450 (3 x 150) plants. Treatments (3 clones x 3 rootstocks) were randomly assigned into two blocks in a complete randomized block design with 50 experimental units per treatment. Experimental units were planted in groups of five plants each. For each block, 225 vines were planted in five rows of 45 plants each, spaced 1 m apart within rows and 2 m between rows. Two and one guard vines were planted at the west and east end, respectively, of the 10 trial rows. A vertical single plane three-wire trellis system was used and Savagnin rose was trained to a bilateral cordon and cane pruned (Komar et al. 2007). The vine culture was conventional for a vineyard in Alsace. Mealybug and soft-scale insect vectors of virus species from the genera Vitivirus and Ampelovirus (Gugerli 2003, Martelli and Boudon-Padieu 2006) were not known to occur in the field site and surrounding vineyards, nor were they detected throughout the trial period. Therefore, opportunities for plant-to-plant transmission of viruses, including GLRaV-1 and GVA, were limited during the trial period. Data collection. The number of clusters was counted at harvest and clusters were weighed for each clone/rootstock combination. In addition, berry samples were randomly collected for each clone/rootstock combination and crushed with a hand press to measure soluble sugars with a hand temperature-compensating refractometer and titratable acidity by titration with 0.1 N NaOH to ph 7.0. Pruning wood was weighed in winter for each clone/rootstock combination as a measure of growth during the preceding season. Data on pruning wood, fresh fruit yield, cluster number, and fruit maturity indices were expressed as increases or decreases relative to healthy clonal material. Table 1 Infection status of three V. vinifera cv. Savagnin rose clones selected for this study. Clone/progeny a Virus elimination Viruses and viruslike diseases b Viruses c 511 Control, untreated LR, KSG, RSP, VM, VN GLRaV-1, GVA, RSPaV 511A Heat therapy/apex grafting RSP, VM, VN RSPaV 511B Heat therapy/apex grafting Healthy none a Savagnin rose clone 511 originated from a commercial vineyard in Alsace, France. Progeny obtained by heat treatment combined with in vitro apex grafting on seedling hypocotyls. b Detected by graft indexing. LR: leafroll; KSG: Kober stem-grooving; RSP: rupestris stem-pitting; VM: vein mosaic; VN: vein necrosis. c Detected by DAS-ELISA using specific immunoglobulins for Grapevine leafroll-associated virus 1 (GLRaV-1), Grapevine virus A (GVA), and Rupestris stem pitting-associated virus (RSPaV).
3 70 Komar et al. Statistical analysis. Data collected on cane pruning weight, yield, number of clusters, fruit soluble sugars, and fruit juice titratable acidity were summarized to obtain descriptive statistical parameters. Analysis of variance (ANOVA) was used to detect treatment differences and relationships between variables with SAS (Statistical Analysis System, SAS Institute Inc., Cary, NC). The means least squares (LS) method was used to compare treatments (511B vs. 511, 511B vs. 511A, and 511 vs. 511A) and to determine differential effects of viral infection status and rootstock genotype combination on field performance. Results Test material and selective virus elimination. The infection status of test vines was assessed by biological indexing and DAS-ELISA before and after virus elimination. Plants of Savagnin rose clone 511 were initially infected by leafroll, RSP, KSG, VM, and VN, as shown by graft indexing (Table 1). DAS-ELISA confirmed the presence of GLRaV-1, GVA, and RSPaV in clone 511. Absorbance values were clearly greater for infected samples than for healthy leaf samples, with OD 405nm readings of ± versus ± for GLRaV-1, ± versus ± 0.29 for GVA, and ± versus ± for RSPaV after substrate hydrolysis for 1.5 hr. After sanitation and indexing, it was determined that leafroll and KSG were eliminated in some Savagnin progeny, including clone 511A, while leafroll, RSP, KSG, VM, and VN were eliminated in other progeny, including clone 511B (Table 1). DAS-ELISA confirmed the presence of RSPaV in clone 511A. Also, the selective elimination of GLRaV-1 and GVA in clone 511A and of GLRaV-1, GVA, and RSPaV in clone 511B was confirmed by DAS-ELISA. Plants of clone 511B were used as a healthy control throughout the study. Susceptibility of rootstock C. The rootstock C exhibited typical stem-pitting symptoms below the graft union when grafted with Savagnin rose clones 511 and 511A but not with clone 511B (data not shown). Symptoms were identical to those observed on V. rupestris. In addition, C did not exhibit symptoms when grafted with GVA-infected, RSPaV-free budwood material, such as Chardonnay clone 76 and Savagnin rose clone 511D (data not shown). These results demonstrate that C is susceptible to RSP but not to KSG. Comparative effect of virus combinations on vigor. Savagnin rose material that was untreated or heat-treated for virus elimination (Table 1) was grafted onto certified rootstocks Kober 5BB, C, or V. rupestris. Test plants were established in the field on 23 Aug 1994 and pruning wood weight was determined over a six-year period ( ). No significant infection status x rootstock interaction (F = 1.25, df = 4, p = 0.29) was observed. The main effects were due primarily to year (F = , df = 5, p < ) and infection status (F = 47.53, df = 2, p < ). A comparative performance analysis of clones 511 and 511A indicated that the selective elimination of GL- RaV-1 and GVA increased vegetative growth by 16 to 31% (Table 2). Overall, the cumulative pruning wood weight decreased significantly (19 to 23%) in clone 511 relative to clone 511B but was not significantly different between clone 511A and clone 511B over six years. Also, there was no significant difference in the vigor of clones 511A grafted onto V. rupestris, C, or Kober 5BB. Similarly, there was no significant difference in the vigor of clone 511 grafted on the three rootstocks. Comparative effect of virus combinations on fruit production. There was no significant infection status x rootstock interaction for yield (F = 0.42, df = 4, p = 0.79), Table 2 Effect of virus combinations on the viticultural performance of V. vinifera cv. Savagnin rose grafted onto three rootstock genotypes over six consecutive years ( ). Vigor (kg/vine) b Production (kg/vine) b Cluster number/vine b Yield/cluster (kg) b Scion/clone/ rootstock (n) a Viral infection status Pruning wood % c Fruit yield % c Weighted mean % c Weighted mean % c 511 5BB (50) GLRaV-1+GVA+RSPaV+VM+VN 2.75 ± 0.42* ± 2.61* ± 4.3* ± 0.001* C (50) GLRaV-1+GVA+RSPaV+VM+VN 1.76 ± 0.46** ± 2.94* ± 4.9* ± 0.002* -28 V. rup. (50) GLRaV-1+GVA+RSPaV+VM+VN 3.06 ± 0.42* ± 2.17* ± 4.3* ± 0.001* A 5BB (50) RSPaV+VM+VN 3.79 ± ± ± ± C (50) RSPaV+VM+VN 2.61 ± ± ± ± V. rup. (50) RSPaV+VM+VN 3.66 ± ± ± ± B 5BB (50) Healthy 3.58 ± 0.53 na ± 4.32 na 27 ± 4.6 na ± na C (50) Healthy 2.79 ± 0.52 na ± 3.88 na 24 ± 4.7 na ± na V. rup. (50) Healthy 3.78 ± 0.55 na ± 2.47 na 28 ± 3.2 na ± na a n: number of vines tested. Plants established in the field in b Cumulative pruning wood weight (kg/vine), cumulative fresh fruit yield (kg/vine), and weighted mean of cluster number per vine and weighted mean of fresh fruit yield per cluster (kg) were measured from 1999 to Data expressed as mean ± standard deviation. Significant differences among means relative to clone 511B are indicated by 5% (*) and 1% (**) LSD. c Percent increase (+) or decrease (-) relative to cumulative growth of respective control vines 511B; na: not applicable.
4 Combined Effect of Rootstock and Virus on Vine Performance 71 cluster number (F = 1.31, df = 4, p = 0.27), and mean yield per cluster (F = 0.61, df = 4, p = 0.66) over a six-year period ( ). The infection status accounted for most variation in yield (F = , df = 2, p < 0.001), cluster number (F = , df = 2, p < 0.001), and yield per cluster (F = , df = 2, p < 0.001) with a significant detrimental impact for virus combination 1 but not for virus combination 2 (Table 2). Furthermore, there was no significant difference in yield, cluster number, and yield per cluster among clone 511 grafted onto Kober 5BB and the other two rootstocks. Likewise, no significant difference in yield, cluster number, and yield per cluster was obtained between clones 511 and 511A grafted onto V. rupestris, C and Kober 5BB. Nonetheless, while cumulative fruit yield decreased significantly (42 to 54%) in clone 511 relative to clone 511B, the fruit yield of clone 511A was not significantly different from clone 511B over six years. A comparative yield analysis of clones 511 and 511A suggested that the selective elimination of GLRaV-1 and GVA increased production by 42 to 50%. Comparative effect of virus combinations on fruit maturity. No significant infection status x rootstock genotype interaction was observed for fruit maturity indexes, such as juice sugar content (F = 0.43, df = 4, p = 0.79) and titratable juice acidity (F = 0.41, df = 4, p = 0.80). There was no significant difference among the three Savagnin rose clones and the rootstock genotype (Table 3). Discussion Scion grape cultivars are grafted onto rootstocks in most vineyards worldwide to protect vines from soil pests, including phylloxera (Daktulosphaira vitifoliae Fitch) and nematodes. Grafting also improves tolerance to abiotic stresses and increases the survival of scion material. Viruses and viruslike diseases can cause substantial production losses, although symptoms are often subtle, particularly for viruses associated with the rugose wood disease complex and those associated with leafroll in white-berried cultivars (Golino 1993, Mannini 2003). Nonetheless, latent infections can be of economic significance over the lifespan of a vineyard because of cumulative annual yield reduction. In our study, no association was found between the vegetative growth and fruit production of Savagnin rose clones infected by virus combination 1 (GLRaV-1, GVA, RSPaV, VN, and VM) or virus combination 2 (RSPaV, VN, and VM) and the rootstock genotype. There was no interaction between the infection status and rootstock genotypes susceptible to KSG and RSP, two major syndromes of the rugose wood disease complex, and the viticultural performance of virus-infected scions. One might intuitively anticipate a close relationship between disease susceptibility and low vigor and production. Our data did not support this hypothesis. Instead, our findings are in agreement with those that show that variation in susceptibility to rugose wood disease does not always account for differences in yield among rootstock-scion combinations (Credi et al. 1991). In other words, low disease severity is not strictly associated with high productivity, suggesting that symptom severity is not an accurate predictor for high-yield rootstock-scion combinations, as previously indicated (Credi and Babini 1996). It would be interesting to expand on these earlier studies and our findings to determine the interaction of other viruses and/or viruslike diseases with rootstock genotype on the performance of infected scion cultivars. The effect of single viruses or single viruslike diseases was not determined in our study because experimental material infected solely with GLRaV-1, GVA, or RSPaV was not available. Instead, the impact of mixed infections by viruslike diseases (vein mosaic and vein necrosis) and virus combinations 1 (GLRaV-1, GVA, and RSPaV) and 2 (RSPaV) was studied. Nonetheless, a comparative performance analysis of clones 511A (RSPaV, VM, and VN) and Table 3 Effect of virus combinations on fruit juice maturity of V. vinifera cv. Savagnin rose grafted onto three rootstocks over six consecutive years ( ). Plants established in the field in Sugar content b Titratable acidity b Scion/clone/rootstock (n) a Viral infection status Brix % c (g/l) % c 511 5BB (50) GLRaV-1+GVA+RSPaV+VM+VN 19.8 ± ± C (50) GLRaV-1+GVA+RSPaV+VM+VN 19.7 ± ± V. rup. (50) GLRaV-1+GVA+RSPaV+VM+VN 20.2 ± ± A 5BB (50) RSPaV+VM+VN 19.2 ± ± C (50) RSPaV+VM+VN 19.3 ± ± V. rup. (50) RSPaV+VM+VN 19.5 ± ± B 5BB (50) Healthy 19.3 ± 1.03 na 5.15 ± 0.48 na C (50) Healthy 19.4 ± 0.93 na 4.77 ± 0.39 na V. rup. (50) Healthy 19.5 ± 0.87 na 5.07 ± 0.56 na a n: number of vines tested. b Soluble solids and titratable acidity measured from 1999 to Data are expressed as mean ± SD. No significant differences among means were found relative to clone 511B. c Percent increase (+) or decrease (-) relative to the healthy control 511B vines; na: not applicable.
5 72 Komar et al. 511B (healthy) showed a limited impact, if any, of RSPaV combined with VM and VN on the viticultural performance of Savagnin rose. These results are consistent with other reports (Credi and Babini 1996, Legin et al. 1993, Reynolds et al. 1997). The fact that RSPaV, VN, and VM have no marked detrimental impact on the vegetative growth and fruit yield across scion cultivars, rootstock genotypes, and environments (northern France, northern Italy, and Canada) does not support the need to include detection assays for this virus and viruslike diseases into certification programs. GLRaV-1 associated with GVA in virus combination 1 reduced vigor and fruit yield but not fruit quality of Savagnin rose. Similar results were reported for V. vinifera cvs. Albana and Trebbiano (Credi and Babini 1996) and Albariño (Mannini 2003). The elimination of GLRaV-1 by itself or in association with Grapevine fleck virus affected titritable acidity but not soluble sugars of Chardonnay (Komar et al. 2007). In our study, yearly fluctuations were observed for most parameters measured except pruning wood, which consistently decreased over time. The best predictors of the effect of virus combination 1 on the viticultural performance of Savagnin rose were cluster number followed by fruit yield and fruit yield per cluster. Interestingly, values for pruning wood weight, cluster number, and juice titratable acidity were very low in 2003, a season that was unusually hot and dry in Alsace, while values for soluble sugars were normal (data not shown). Kober 5BB and C are both moderately vigorous rootstocks whereas V. rupestris is highly vigorous. Despite a differential intrinsic vigor, there were no significant differences attributable to rootstock on the viticultural performance of virus-infected Savagnin rose, although slightly reduced vegetative growth was observed on C for scion material infected with virus combination 1. A similar conclusion was reached by comparing the growth of three V. berlandieri x V. riparia rootstocks infected with viruses and viruslike diseases for which vigor varied from moderate (Kober 5BB and 420 A) to high (Teleki 5A) (Credi and Babini 1996). To the best of our knowledge, our study is the first comparative impact analysis of different rootstocks on the performance of clonal V. vinifera scions with distinct infection status. Since our test material was genetically homogeneous, there was limited variability in vine performance because of genetic factors. Also, uncharacterized viruses and/or viruslike agents, if present in Savagnin rose clone 511, had limited, if any, impact on the performance of the test material because of its genetic homogeneity. Conclusion Our findings were consistent with no interaction between viruses associated with leafroll, KSG, and RSP diseases and rootstock genotypes susceptible to KSG and RSP (Kober 5BB, V. rupestris, and C) on the viticultural performance of infected V. vinifera cv. Savagnin rose scions. Also, RSPaV, vein mosaic, and vein necrosis had limited, if any, impact on vigor, production, and fruit maturity of V. vinifera cv. Savagnin rose. Literature Cited Abou Ghanem-Sabanadzovic, N., S. Sabanadzovic, J.K. Uyemoto, and A. Rowhani A putative new ampelovirus associated with grapevine leafroll disease. In 15th Meeting of the International Council for the Study of Virus and Virus-like Diseases of the Grapevine: Extended Abstracts, pp Stellenbosh, South Africa (www. Bass, P., and A. Vuittenez Amélioration de la thermothérapie des vignes virosées au moyen de la culture d apex sur milieux nutritifs ou par greffage sur des vignes de semis obtenues aseptiquement in vitro. Ann. Phytopathol. 9: Borgo, M., N. Bertazzon, F. Anaclerio, and E. Angelini Graft incompatibility and leafroll symptoms in grapevines affected by different GLRaV-2 variants. In 15 th Meeting of the International Council for the Study of Virus and Virus-like Diseases of the Grapevine: Extended Abstracts, pp Stellenbosh, South Africa (www. Credi, R., and A.R. Babini Effect of virus and virus-like infections on the growth of grapevine rootstocks. Adv. Hortic. Sci. 10: Credi, R., O. Silvestroni, A. Santucci, and A. Canova Variation of grapevine rootstock susceptibility to the rugose wood disease legno riccio. Phytopathol. Medit. 30: Golino, D.A Potential interactions between rootstocks and grapevine latent viruses. Am. J. Enol. Vitic. 44: Golino, D.A Emerging grapevine diseases. In 14th Meeting of the International Council for the Study of Virus and Virus-Like Diseases of the Grapevine: Extended Abstracts. G.P. Martelli (ed.), pp Locorotondo, Italy (www. Golino, D.A., S. Sim, and A. Rowhani The role of GLRaV-2 and GVB in virus induced rootstock decline in California grapevines. Phytopathology 90:S28. Golino, D.A., S. Sim, and A. Rowhani The role of rootstock genotype in the effects of single and mixed infections of grapevine viruses. In 14th Meeting of the International Council for the Study of Virus and Virus-Like Diseases of the Grapevine: Extended Abstracts. G.P. Martelli (ed.), pp Locorotondo, Italy (www. Greif, C., and B. Walter The European reference collection of grapevine virus diseases. In Sanitary Selection of the Grapevine. Protocols for Detection of Viruses and Virus-like Diseases. B. Walter (ed.), pp INRA Editions, Paris. Greif, C., R. Garau, D. Boscia, V.A. Prota, M. Fiori, P. Bass, B. Walter, and U. Prota The relationship of grapevine leafroll-associated virus 2 with a graft incompatibility condition of grapevines. Phytopathol. Medit. 34: Gugerli, P Grapevine leafroll and related viruses. In 14th Meeting of the International Council for the Study of Virus and Virus-Like Diseases of the Grapevine: Extended Abstracts. G.P. Martelli (ed.), pp Locorotondo, Italy (www. Komar, V., E. Vigne, G. Demangeat, and M. Fuchs Beneficial effect of selective virus elimination on the performance of Vitis vinifera cv. Chardonnay. Am. J. Enol. Vitic. 58: Legin, R., P. Bass, L. Etienne, and M. Fuchs Selection of mild virus strains of fanleaf degeneration by comparative field performance of infected grapevines. Vitis 32: Mannini, F Virus elimination in grapevine and crop performance. In 14th Meeting of the International Council for the Study
6 Combined Effect of Rootstock and Virus on Vine Performance 73 of Virus and Virus-Like Diseases of the Grapevine: Extended Abstracts. G.P. Martelli (ed.), pp Locorotondo, Italy (www. Martelli, G.P Grapevine virology highlights In 15th Meeting of the International Council for the Study of Virus and Virus-like Diseases of the Grapevine: Extended Abstracts, pp Stellenbosh, South Africa (www. Martelli, G.P., and E. Boudon-Padieu Directory of infectious diseases of grapevine and viruses and virus-like diseases of the grapevine. Option Médit. Série B, Studies and Research 55:279. Reynolds, A.G., W.S. Lanterman, and D.A. Wardle Yield and berry composition of five Vitis cultivars as affected by Rupestris stem pitting virus. Am. J. Enol. Vitic. 48: Rowhani, A., J.K. Uyemoto, D.A. Golino, and G.P. Martelli Pathogen testing and certification of Vitis and Prunus species. Ann. Rev. Phytopathol. 43: Uyemoto, J.K., and Rowhani, A Discovery of different grapevine sources with graft-transmissible agents causing union-incompatibility on sensitive rootstocks. In 14th Meeting of the International Council for the Study of Virus and Virus-Like Diseases of the Grapevine: Extended Abstracts. G.P. Martelli (ed.), pp Locorotondo, Italy (www. Walter, B., and L. Etienne Detection of the grapevine fanleaf viruses away from the period of vegetation. J. Phytopathol. 120: Walter, B., P. Bass, R. Legin, C. Martin, R. Vernoy, A. Collas, and G. Vesselle The use of a green-grafting technique for the detection of virus-like diseases of the grapevine. J. Phytopathol. 128: Zimmermann, D., G. Sommermeyer, B. Walter, and M.H.V. Van Regenmortel Production and characterization of monoclonal antibodies specific to closterovirus-like particles associated with grapevine leafroll disease. J. Phytopathol. 130:
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