Grapevine viruses – a global challenge and biotechnological solutions to obtain healthy material
DOI:
https://doi.org/10.51258/RJH.2025.05Keywords:
Vitis, GFLV, GLRaVs, GFkV, economic effects, virus-eliminationAbstract
Grapevine (Vitis spp.) is one of the most important horticultural species, but also one of the most vulnerable to viral infections. To date, 102 viruses are known to infect grapevines. Of these, some viruses cause significant economic damage worldwide, affecting the quantity and quality production, plant growth and development, and the vineyards long-lasting. Other viruses have a broad spectrum, affecting several crop plants and represent scientific curiosities for the grapevine, both because they are rarely encountered and the damages induced are negligible. This paper summarizes the main knowledge regarding the diversity of viral agents affecting grapevine and the associated symptomatology characteristics. The economic effects of viral diseases are analyzed, highlighting their influence on propagation material and grape production. Once virus-infected, grapevine plants remain infected for their entire life. Prevention of infection includes the production of certified virus-free planting material and virus testing. Thus, the propagation of healthy material, originating from authorized sources, tested and certified as virus-free, is essential for sustainable viticulture. Also, virus-elimination methods are presented (meristem/shoot tip cultures, thermotherapy, in vitro chemotherapy, electrotherapy, cryotherapy, and combined methods), which allow the regeneration of healthy, virus-free plants. The integration of these technologies into virus-free germplasm selection and conservation programs represents a priority direction for a modern viticulture, ensuring the maintenance of grapevine health, the protection of genetic diversity and the sustainability of grapevine production.
Downloads
References
Al Rwahnih, M., Daubert, S., Golino, D. and Rowhani, A. (2009). Deep sequencing analysis of RNAs from a grapevine showing Syrah decline symptoms reveals a multiple virus infection that includes a novel virus. Virology 387, 395–401.
Altmayer, B. (1989). Investigations on the elimination of nepovirus and Grapevine leafroll by shoot tip meristem culture of grape virus. Phytoparasitica 17, 72-73.
Angelini, E., Bertazzon, N. and Borgo, M. (2001). Sensitivity of grapevine rootstocks to GFkV infection. Phytopathol. Mediterr. 40 (Suppl.), 423–428.
Atallah, S.S., Gomez, M.I., Fuchs, M.F. and Martinson, T.E. (2012). Economic impact of Grapevine leafroll disease on Vitis vinifera cv. Cabernet Franc in Finger Lakes vineyards of New York. Am. J. Enol. Vitic. 63, 73–79.
Barba, M., Martino, L. and Cupidi, A. (1992). Il rasanamento della vite: tre tecniche a confronto (Grapevine sanitation: three methods compared). Vignevini 19(3), 33-36.
Barlass, M., Skene, K.G.M., Woodham, R.C. and Krake, L.R. (1982). Regeneration of virus free grapevines using in vitro apical culture. Ann. Appl. Biol. 101, 291-295.
Bayati, S., Shams-Bakhsh, M. and Moieni, A. (2011). Elimination of Grapevine virus A(GVA) by cryotherapy and electrothera¬py. J. Agric. Sci. Technol. 13, 443-450.
Bell, V.A., Blouin, A.G., Cohen, D., Hedderley, D.I., Oosthuizen, T., Spreeth, N.A., Lester, P.J. and Pietersen, G. (2017). Visual symptom identification of Grapevine leafroll associated virus 3 in red berry cultivars supports virus management by roguing. J. Plant Pathol. 99, 477-482.
Bertamini, M., Malossini, U., Muthuchelian, K. and Nedunchezhian, N. (2005). Physiological response of field grown grapevine (Vitis vinifera L. cv. Marzemino) to Grapevine leafroll-associated virus (GLRaV-1). Phytopathol. 44(3), 256–265.
Bertazzon, N., Filippin, L., Forte, V. and Angelini, E. (2017). Grapevine Pinot gris virus: a threat for European viticulture. Eur. J. Plant Pathol. 149, 929–943. https://doi.org/10.1007/s10658-017-1222-1.
Bettoni, J.C., Costa, M.D., Gardin, J.P.P., Kretzschmar, A.A. and Pathirana, R. (2016). Cryotherapy: a new technique to obtain grapevine plants free of viruses. Rev. Bras. Frutic. 38:e- 833.
Bi, W.-L., Hao, X.-Y., Cui, Z.-H., Pathirana, R., Volk, G.M. and Wang, Q.-C. (2018). Shoot tip cryotherapy for efficient of Grapevine leafroll-associated virus-3 from diseased grapevine in vitro plants. Ann. Appl. Biol. 173, 261-270.
Bittner, H., Schenk, G., Schuster, G. and Kluge, S. (1989). Elimination by chemotherapy of Potato virus S from potato plants grown in vitro. J. Potatos Research 32(2), 175-179.
Bovey, R. and Martelli, G.P. (1992) Directory of Major Virus and Virus-Like Diseases of Grapevines. MFCIC and ICVG, 111 pp.
Buciumeanu, E. and Vișoiu, E. (1996). Elimination of Grapevine leafroll associated virus type III by heat treatment and in vitro culture. In Current problems and techniques in cellular and molecular biology (Timișoara, Romania: Mirton Publishing House), pp. 626-631.
Burger, J.G. (1989). Electrotherapy: a possible method to eliminate Grapevine fanleaf virus from grapevine. Paper presented at: 9th ICVG (Kiryat Anavim, Israel, 1987).
Cheplick, S.M. and Agrios, G.N. (1983). Effect of injected antiviral compounds on Apple mosaic, scar skin and apple diseases of apple trees. Plant Dis. 67, 1130-1133.
Cieniewicz, E.J., Qiu, W., Saldarelli, P. and Fuchs, M. (2020). Believing Is Seeing: Lessons from Emerging Viruses in Grapevine. J. Plant Pathol. 102, 619–632.
Clark, M. and Adams, A. (1977). Characteristics of the microplate method of enzyme-linked immunosorbent assay for the detection of plant viruses. J. Gen. Virol. 34(3), 475-483.
Corbetta, M.K., Kasdorf, G.G.F., Engelbrecht, D.J. and Wiid, J. (1984). Detection of viral-like particles by electron microscopy of negatively stained extracts from grapevines. S. Afr. J. Enol. Vitic. 5(2), 43-49.
Cui, Z.H., Agüero, C.B., Wang, Q.C. and Walker, M.A. (2019). Validation of micrografting to identify incompatible interactions of rootstocks with virus-infected scions of Cabernet Franc. Aust. J. Grape Wine Res. 25, 268–275.
Cuozzo, D., Chitarra, W., Ferrandino, A., Gribaudo, I., Gambino, G. and Mannini, F. (2018). Field performances and grape quality of the same clone of ʻNebbiolo’ (Vitis vinifera L.) when infected by GLRaV-1+GVA, GVA or healthy. Paper presented at:19th ICVG (Santiago, Chile).
De Fazio, G., Caner, J. and Vicente, M. (1978). Inhibitory effect of Virazole (Ribavirin) on the replication of Tomato White Necrosis – Virus (VNBT). Arch. Virol. 58, 153-156.
Engel, A.K. and Fries, P. (2010). Beta-band oscillations-signalling the status quo? Curr. Opin. Neurobiol. 20(2), 156-165.
Faccioli, V.C. and Marani, F. (1998). Virus elimination by meristem tip culture and tip micrografting. In Plant virus disease control (St. Paul: APS Press), pp. 346-380.
Fayek, M.A., Jomaa, A.H., A Shalaby, A.-B. and Al-Dhaher, M.-M. (2009). Meristem tip culture for in vitro eradication of Grapevine leafroll- associated virus-1 (GLRaV-1) and Grapevine fan leaf virus (GFLV) from infected flame seedless grapevine plantlets. Ini. Inv., 4:al, ISSN-e 1988-415X.
Fuchs, M. (2020). Grapevine viruses: a multitude of diverse species with simple but overall poorly adopted management solutions in the vineyard. J. Plant Pathol. 102, 643–653. https://doi.org/10.1007/s42161-020-00579-2.
Fuchs, M. (2023). Grapevine virology highlights: 2018-2023. Paper presented at: 20th ICVG (Thessaloniki, Greece).
Fuchs, M. (2025). Grapevine viruses: Did you say more than a hundred? J. Plant Pathol. 107, 217–227. https://doi.org/10.1007/s42161-024-01819-5.
Fuchs, M., Almeyda, C.V., Al Rwahnih, M., Atallah, S.S., Cieniewicz, E.J., Farrar, K., Foote, W.R., Golino, D.A., Gómez, M.I., Harper, S.J. et al. (2021). Economic studies reinforce efforts to safeguard specialty crops in the United States. Plant Dis. 105, 14–26.
Garau, R., Fiori, P.P., Prota, V.A., Tolu, G., Fiori, M. and Prota, U. (1997). Effect of virus infection on own-rooted clones of different wine grapes cultivars from Sardinia. Paper presented at: 12th ICVG (Lisbon, Portugal).
Giampetruzzi, A., Roumi, V., Roberto, R., Malossini, U., Yoshikawa, N., La Notte, P., Terlizzi, F., Credi, R., Saldarelli, P.A. (2012). New grapevine virus discovered by deep sequencing of virus-and viroid-derived small RNAs in cv. Pinot gris. Virus Res. 163(1): 262–8. https:// doi. org/ 10. 1016/j. virus res. 2011. 10. 010.
Golino, D.A., Rowhani, A., Klaassen, V., Sim, S.T. and Al Rwahnih, M. (2015). Grapevine leafroll-associated virus 1 effects on different grapevine rootstocks. Paper presented at: 18th ICVG (Ankara, Turkey).
Golino, D.A., Sim, S. and Rowhani, A. (2003). The role or rootstock genotype in the effects of single and mixed infections of grapevine viruses. Paper presented at: 14th ICVG (Locorotondo, Bari, Italy).
Gonzales, J.E., Sanchez, R. and Sanchez, A. (2006). Biophysical analysis of electric current mediated nucleoprotein inactivation process. Eprint arXiv.q-bio/0601014. Paper presented at: First International Workshop on Bioinformatics (Santa Clara, Cuba – Flanders).
Goussard, P.G., Wiid, J. and Kasdorf, G.G.F. (1991). The effect of in vitro somatic embryogenesis in eliminating fanleaf virus and leafroll associated viruses from grapevines. S. Afr. J. Enol. Vitic. 12, 77-81.
Gribaudo, I., Gambino, G., Cuozzo, D. and Mannini, F. (2006). Attempts to eliminate Grapevine Rupestris Stem Pitting-Associated Virus from grapevine clones. J. Plant Pathol. 88(3), 293-298.
Guţă, I.-C. and Buciumeanu, E.-C. (2010). Utilizarea chimioterapiei in vitro pentru eliminarea infecţiilor virale multiple la viţa de vie. Paper presented at: A XXVIII-a sesiune ştiinţifică a SNBC (Constanța, Romania).
Guţă, I.-C. and Buciumeanu, E.-C. (2011). Grapevine chemotherapy for elimination of multiple virus infection. Rom. Biotechnol. Lett. 16(5), 6535-6539.
Guţă, I.-C. and Buciumeanu, E.-C. (2012). Chemotherapy and electrotherapy: environmental friendly methods for virus elimination in grapevine. Paper presented at: 14th Serbian congress of fruit and grapevine producers with international participation (Vrnjačka Banja, Serbia).
Guță, I.-C. and Buciumeanu, E.-C. (2021). Quality improvement of the grapevine planting stock through virus elimination by in vitro chemotherapy. RJH 2(1), 17-22.
Guţă, I.-C., Buciumean,u E.-C., Gheorghe, R.N. and Teodorescu, Al. (2009a). The assessment of viricides phytotoxicity used in grapevine in vitro chemotherapy. Bulletin UASVM, Horticulture 66(1), 661.
Guţă, I.-C., Buciumeanu, E.-C., Gheorghe, R.N. and Teodorescu, AL. (2009b). Examination of phytotoxic effect of viricides on grapevine in controlled medium. Scientifical Papers USAMVB, Serie B, Horticulture, Vol. LIII, 559-563.
Guţă, I.-C., Buciumeanu, E.-C., Gheorghe, R.N. and Teodorescu, AL. (2010). Solutions to eliminate Grapevine leafroll associated virus serotype 1+3 from V. vinifera L. cv. Ranâi Magaraci. Rom. Biotechnol. Lett. 15(1) (Suppl.), 72-78.
Guţă, I.-C., Buciumeanu, E.-C., Oprescu, B. and Tătaru, L. (2011). Effect of direct electric current on virus elimination in grapevine. Paper presented at: 4th International Symposium New Researches in Biotechnology Simp BTH 2011 (Bucharest, Romania).
Guţă, I.-C., Buciumeanu, E.-C. and Sumedrea, D.I. (2025). Using the analytical hierarchy process to select the most appropriate method for grapevine Pinot gris virus and Grapevine fleck virus elimination. Acta Hortic. 1418, 151-158. https://doi.org/10.17660/ActaHortic.2025.1418.19.
Guţă, I.-C., Buciumeanu, E.-C., Tătaru, L.D., Oprescu, B, and Topală, C.M. (2019). New approach of electrotherapy for grapevine virus elimination. Acta Hortic. 1242, 697-702. DOI: 10.17660/ActaHortic.2019.1242.103.
Guţă, I.-C., Buciumeanu, E.-C., Tătaru, L.D. and Topală, C.M., (2017a). Regeneration of grapevine virus-free plants by in vitro chemotherapy. Acta Hortic. 1188, 319-322. DOI 10.17660/ActaHortic.2017.1188.42.
Guţă, I.-C., Buciumeanu, E.-C., Topală, C.M. and Tătaru, L.D. (2017b). The use of in vitro chemotherapy in grapevine virus elimination. Acta Hortic. 1155, 425-430. DOI:10.17660/ActaHortic.2017.1155.63.
Guţă, I.-C., Buciumeanu, E. and Vişoiu, E. (2008a). Evaluarea activităţii ribavirinei asupra proceselor de regenerare şi devirozare in vitro la viţa de vie. In Cachiță-Cosma D., Brezeanu A., Ardelean A. (Coord.), Biotehnologii vegetale pentru secolul XXI. Cluj-Napoca: Ed. Risoprint, 95-101.
Guţă, I.-C., Buciumeanu, E.-C. and Vişoiu, E. (2014). Elimination of Grapevine fleck virus by in vitro chemotherapy. Not. Bot. Horti. Agrobo. 42(1), 115-118.
Guţă, I.-C., Buciumeanu, E.-C., Vişoiu, E., Teodorescu, Al. and Liţă, I. (2008b). The possibility of grapevine virus free regeneration in the presence of electric field. Paper presented at: XXXVIII ESNA Annual Meeting (Krakow, Poland).
Guţă, I.-C., Buciumeanu, E.-C., Vişoiu, E., Teodorescu, Al. and Liţă, I. (2008c). The effect of electric field on in vitro regenerative processes and grapevine virus elimination. Lucrări ştiinţifice Seria B-LI-2008 Horticultură, 482-486.
Habili, N., Wu, Q. and Pagay, V. (2016). Virus-associated Shiraz Disease may lead Shiraz to become an endangered variety in Australia. Wine Vitic. J. 31, 47–50.
Hatzinikolakis, H.K. and Roubelakis-Angelakis, K.A. (1993). A modified method for in vitro thermotherapy and meristem culture for production of virus-free grapevine plant material. Paper presented at: 11th ICVG (Montreux, Switzerland).
Hao, X.-Y., Jiao, B.-L., Wang, M.-R., Wang, Y.-L., Shang, B.-X., Wang, J.-Y., Wang ,Q.-C. and Xu, Y. (2021). In vitro biological indexing of Grapevine leafroll-associated virus 3 in red- and white-berried grapevines (Vitis vinifera). Aust. J. Grape Wine Res. 27, 483–490. https://doi.org/10.1111/ajgw.12505.
Helliot, B., Panis, B., Locicero, A., Reyniers, K., Muylle, H., Vandewalle, M., Michel, C., Swennen, R. and Lepoivre, P. (2001). Development of in vitro technique for the elimination of cucumber mosaic virus from Musa. Acta Hortic. (ISHS) 560, 535-538. DOI: 10.17660/ActaHortic.2001.560.109.
Hily, J.-M., Poulicard, N., Candresse, T., Vigne, E., Beuve, M., Renault, L., Velt, A., Spilmont, A.-S. and Lemaire, O. (2020). Datamining, Genetic Diversity Analyses, and Phylogeographic Reconstructions Redefine the Worldwide Evolutionary History of Grapevine Pinot Gris Virusand Grapevine Berry Inner Necrosis Virus. Phytobiomes J. 4, 165–177.
Hu, G.-J., Dong, Y., Zhang, Z., Fan, X. and Ren, F. (2020). Efficiency of chemotherapy combined with thermotherapy for eliminating Grapevine leafroll-associated virus 3(GLRaV-3). Sci. Hortic. 271, 109462.
Hu, G.-J., Dong, Y.-F., Zhang, Z.-P., Fan, X.-D. and Ren, F. (2021). Elimination of Grapevine fleck virus and Grapevine rupestris stem pitting-associated virus from Vitis vinifera 87-1 by riba¬virin combined with thermotherapy. J. Integr. Agric. 20, 2463- 2470.
Igarza Castro, J., Hernandez, P.R. and Cruz Castelanos, B. (2001). Electrotherapy as an alternative for elimination of DMW virus in tania. Manejo integrado de plagas 60, 57-60.
Leonhardt, W., Wowrosch, Ch., Auer, A. and Koop, B. (1998). Monitoring of virus diseases in Austrian grapevine varieties and virus elimination using in vitro thermotherapy. Plant Cell, Tissue and Organ Culture 52, 71-74.
Kappagantu, M., Collum, T.D., Dardick, C. and Culver, J.N. (2020). Viral Hacks of the Plant Vasculature: The Role of Phloem Alterations in Systemic Virus Infection. Ann. Rev. Virol. 7(1), 351-370.
Komínek, P., Komíneková, M. and Jandová, B. (2016). Effect of repeated Ribavirin treatment on grapevine viruses. Acta virologica 60, 400-403, doi: 10.4149/av_2016_04_400.
Koruza, B. and Jelaska, S. (1993). Influence of meristem culture and virus elimination on phenotypical modifications of grapevine (Vitis vinifera L., cv. Refošk). Vitis 22, 59-60.
Krake, L.R., Scott, N.S., Rezaian, M. and Taylor, R. (1999). Graft-Transmitted Diseases of Grapevines (Collingwood, Australia: CSIRO Publishing), pp. 137.
Křižan, B., Moravcová, K., Ondrušiková, E., Adam, E., Holleinová, V. and Pidra, M. (2008). Thermotherapy of grapevines and apricots by reason of viruses and phytoplasma elimination. Acta Hortic. 781, 93-96.
Křižan, B., Moravcová, K., Ondrušiková, E., Adam, E., Holleinová, V. and Bláhová, L. (2009). Elimination of grapevine fanleaf virus in grapevine by in vivo and in vitro thermotherapy. Hort. Sci. 36(3), 105-108.
Mahlein, A.K. (2016). Plant disease detection by imaging sensors - Parallels and specific demands for precision agriculture and plant phenotyping. Plant Dis. 100, 241–251.
Malagnini, V., de Lillo, E., Saldarelli, P., Beber, R., Duso, C., Raiola, A., Zanotelli, L., Valenzano, D., Giampetruzzi, A., Morelli, M. et al. (2016). Transmission of Grapevine Pinot gris virus by Colomerus vitis (Acari: Eriophyidae) to grapevine. Arch. Virol. 161(9), 2595-9.
Maliogka, V.I., Martelli, G.P., Fuchs, M. and Katis, N.I. (2015). Control of viruses infecting grapevine. Adv. Virus Res. 91, 175-227.
Maliogka, V.I., Skiada, F.G., Eleftheriou, E.P. and Katis, N.I. (2009). Elimination of a new ampelovirus (GLRaV-PR) and Grapevine rupestris stem pitting-associated virus (GRSPaV) from two Vitis vinifera cultivars combining in vitro thermo-therapy with shoot tip culture. Sci. Hortic. 123, 280-282.
Malossini, U., Bianchedi, P., Villegas, T.R., Varner, M., Gualandri, V. and Nicolini, G. (2014). An updating about the performances of Pinot Gris and Traminer vines affected by the GPGV trichovirus-related grapevine disease. Paper presented at: 37th World Congress of Vine and Wine (Mendoza, Argentina).
Malossini, U., Ciccotti, A.M., Bragagna, P., Vindimian, M.E., Moser, S., Versini, G., and Nicolini, G. (2003). Changes in agronomical and oenological performances of clones of the grapevine cv Gewürztraminer after GFLV elimination by heat therapy. Paper presented at: 14th ICVG (Locorotondo, Bari, Italy).
Mannini, F. (2003). Virus elimination in grapevine and crop performance. Paper presented at: 14th ICVG (Locorotondo, Bari, Italy).
Manu, V. and Manju, M. (2018). Elimination of viruses through thermotherapy and meristem culture in apple cultivar „Oregon Spur-II”. Virus diseases 29(1), 75-82
Marković, Z., Preiner, D., Stupić, D., Andabaka, Ž., Šimon, S., Vončina, D., Maletić, E., Kontić, J.K., Chatelet, P. and Engel¬mann, F. (2015). Cryopreservation and cryotherapy of grape¬vine (Vitis vinifera L.). Vitis 54, 247-251.
Martelli, G.P. (1999). Infectious diseases and certification of grapevines. In Proceedings of the Mediterranean network on grapevine closteroviruses 1992-1997 and the viroses and virus-like diseases of the grapevine a bibliographic report, 1985-1997. Options méditerranéennes, Série A Nr. 29 (Bari, Italy: CIHEAM), pp. 47-64.
Martelli, G.P. and Gallitelli, D. (2008). Emerging and Reemerging Virus Diseases of Plants. In Encyclopedia of Virology, 3rd edn. pp. 86-92. https://doi.org/10.1016/B978-012374410-4.00705. Academic Press.
Martelli G.P. (2014). Directory of virus and virus-like diseases of the grapevine and their agents. J. Plant Pathol. 96, 1–136. http://dx.doi.org/10.4454/JPP.V96I1SUP.
Martelli, G.P. (2017). An Overview on Grapevine Viruses, Viroids, and the Diseases They Cause. In Grapevine Viruses: Molecular Biology, Diagnostics and Management. Springer, Cham. pp. 31-46. DOI: 10.1007/978-3-319-57706-7_2.
Martelli G.P. (2018). Where grapevine virology is heading to. Paper presented at: 19th ICVG, (Santiago, Chile).
Martelli, G.P. and Boudon-Padieu, E. (Eds.) (2006). Directory of infectious diseases of grapevines and viroses and virus-like diseases of the grapevine: bibliographic report 1998–2004. In Directory of infectious diseases of grapevines and viroses and virus-like diseases of the grapevine: bibliographic report 1998–2004. Vol. 55. Options méditerranéennes: Série B. Etudes et Recherches (Bari, Italy: CIHEAM), pp. 10-21
Martínez-Lüscher, J., Plank, C.M., Brillante, L., Cooper, M.L., Smith, R.J., Al-Rwahnih ,M., Yu, R., Oberholster, A., Girardello, R. and Kurtural, S.K. (2019). Grapevine Red Blotch Virus May Reduce Carbon Translocation Leading to Impaired Grape Berry Ripening. J. Agric. Food Chem. 67(9), 2437-2448.
Mellor, F.C. and Stace-Smith, R. (1977). Virus-free potatoes by tissue culture. In Applied and fundamental aspects of plant cell, tissue, and organ culture. Germany: Springer-Verlog Publisher. pp. 616-638.
Messmer, N., Bohnert, P., Askani, L., Schumacher, S., Voegele, R.T. and Fuchs, R. (2024). Grapevine Pinot gris virus spreads in infected vineyards: latent infections have no direct impact on grape production. Virol. J. 21(1), 178. doi: 10.1186/s12985-024-02453-4.
Miljanić, V., Rusjan, D., Škvarč, A., Chatelet, P. and Štajner, N. (2022). Elimination of eight viruses and two viroids from preclonal candidates of six grapevine varieties (Vitis vinifera L.) through in vivo thermotherapy and in vitro meristem tip micrografting. Plants 11, 1064.
Minafra, A., Mawassi, M., Goszczynski, D. and Saldarelli, P. (2017). Grapevine Vitiviruses. In Grapevine Viruses: Molecular Biology, Diagnostics and Management. (Springer: Cham, Switzerland), pp. 229–256.
Moutinho-Pereira, J., Correia, C.M., Gonçalves, B., Bacelar, E.A., Coutinho, J.F., Ferreira, H.F., Lousada, J.L. and Cortez, M.I. (2012). Impacts of leafroll-associated viruses (GLRaV-1 and -3) on the physiology of the Portuguese grapevine cultivar ‘Touriga Nacional’ growing under field conditions. Ann. Appl. Biol. 160, 237-249.
Naidu, R.A., Maree, H.J. and Burger, J.T. (2015). Grapevine leafroll disease and associated viruses: a unique pathosystem. Annu. Rev. Phytopathol. 53, 613–634.
Naidu, R.A., Rowhani, A., Fuchs, M., Golino, D.A. and Martelli, G.P. (2014). Grapevine leafroll: a complex viral disease affecting a high-value fruit crop. Plant Dis. 98(9), 1172–1185.
Nascimento, L.C., Pio-Ribeiro, G., Willadino, L. and Andrade, G.P. (2003). Stock indexing and Potato virus elimination from potato plants cultivated in vitro. Scientia Agricola 60(3), 525-530.
Nguyen, C., Sagan, V., Maimaitiyiming, M., Maimaitijiang, M., Bhadras and Kwasniewski, M.T. (2021). Early Detection of Plant Viral Disease Using Hyperspectral Imaging and Deep Learning. Sensors 21(3), 742. https://doi.org/10.3390/s21030742.
Oliver, J.E. and Fuchs, M.F. (2011). Fanleaf degeneration/decline disease of grapevines. Integrated Pests Management. https://ecommons.cornell.edu/server/api/core/bitstreams/ee6242d0-fabc-4085-88b2-19d1ea7fb805/content.
Pacifico, D., Caciagli, P., Palmano, S., Mannini, F. and Marzachì, C. (2011). Quantitation of Grapevine leafroll associated virus-1 and -3, Grapevine virus A, Grapevine fanleaf virus and Grapevine fleck virus in field-collected Vitis vinifera L. ‘Nebbiolo’ by real-time reverse transcription-PCR. J. Virol. Methods 172, 1–7.
Panattoni, A., D’Anna, F., Cristani, C. and Triolo, E. (2007). Grapevine virus A eradication in Vitis vinifera explants by antiviral drugs and thermotherapy. J. Virol. Methods 146, 129-135.
Panattoni, A., Luvisi, A. and Triolo, E. (2013). Review. Elimination of viruses in plants: twenty years of progress. Span. j. agric. res. 11(1), 173–188. https://doi.org/10.5424/SJAR/2013111-3201.
Panattoni, A. and Triolo, E. (2010). Susceptibility of grapevine viruses to thermotherapy on in vitro collection of Kober 5BB. Sci. Hortic. 125, 63-67.
Perrone, I., Chitarra, W., Boccacci, P. and Gambino, G. (2017). Grapevine-virus-environment interactions: an intriguing puzzle to solve. New Phytol. 213(3), 983-987.
Pesqueira, A.M., García-Berrios, J.-J., Barrasa, M. and Cabaleiro, C. (2012). Economic Impact of Leafroll Disease in Vineyards of the Cultivar Albariño in Rías Baixas (Spain). Paper presented at: 17th ICVG (Davis, CA, USA).
Poojari, S., Moreau, D.L., Kahl, D., Ritchie, M., Ali, S. and Úrbez-Torres, J.R. (2020). Disease Incidence and Genetic Variability of Economically Important Grapevine Viruses in Nova Scotia. Can. J. Plant Pathol. 42, 584–594.
Prosser, S.W., Goszczynski, D.E. and Meng, B. (2007). Molecular analysis of double-stranded RNAs reveals complex infection of grapevines with multiple viruses. Virus Res. 124, 151–159.
Quak, F. (1987). Therapy of individual plants. In Viruses of potatoes and seed-potato production, De Bokx J.A., van der Want J.P.H. (Eds.), Wageningen: Pudoc, pp. 151–161.
Rayapati, N. (2017). Risk of virus problems in field-grafted vineyards. Good Fruit Grower/June 6, 2017. https://www.goodfruit.com/rayapati-risk-of-virus-problems-in-field-grafted-vineyards/.
Rayapati, N., Rowhani, A., Fuchs, M., Golino, D. and Martelli, G.P. (2014). Grapevine leafroll: a complex viral disease affecting a high-value fruit crop. Plant Dis. 98, 1172-1185.
Ricketts, K.D., Gomez, M.I., Atallah, S.S., Fuchs, M.F., Martinson, T.E., Battany, M.C., Bettiga, L.J, Cooper ,M.L., Verdegaal, P.S. and Smith, R.J. (2015). Reducing the economic impact of grapevine leafroll disease in California: identifying optimal disease management strategies. Am. J. Enol. Vitic. 66, 138–147.
Rieger, T. (2016). GPGV Pinot gris virus in More Napa Vineyards. Wines and Vines, December 5.
Rowhani, A., Golino, D.A, Klaassen, V., Sim, S.T., Gouran, M. and Al Rwahnih, M. (2015). Grapevine Leafroll associated virus 3: Effects on rootstocks, vine performance, yield and berries. Paper presented at: 18th ICVG (Ankara, Turkey).
Rowhani, A., Uyemoto, J.K., Golino, D.A., Daubert, S.D. and Al Rwahnih, M. (2017). Virus involved in graft incompatibility and decline. In Grapevine Viruses: Molecular Biology, Diagnostics and Management (Springer: Cham, Switzerland), pp. 289–302.
Russo, M. (2005). Electron Microscopy of Grapevine Virus Infections. Phytopathol. Mediterr., 24 (1/2), 144–47.
Saldarelli, P., Giampetruzzi, A., Maree, H.J. and Al Rwahnih, M. (2017). High-Throughput Sequencing: Advantages Beyond Virus Identification. In Grapevine Viruses: Molecular Biology, Diagnostics and Management (Springer: Cham, Switzerland), pp. 625–642.
Saldarelli, P., Giampetruzzi, A., Morelli, M., Malossini, U., Pirolo, C., Bianchedi, P. and Gualandri, V. (2015). Genetic variability of grapevine Pinot gris virus and its association with grapevine leaf mottling and deformation. Phytopathology 105(4), 555-63.
Samaali, B., Toumi, A., Hadamane, A.M. and Kallel, S. (2019). Study of Distribution and Analysis of the Transmission of Grapevine Fanleaf Virus in Northern Tunisian Vineyards. J. New Sci. 64, 4040–4047.
Savino, V., Di Terlizz, B., Rivieccio, S. and Di Silvio, F. (1991). Presence in clonal rootstocks of a graft-transmissible factor that induces stunting and bushy growth in European grapevines. Paper presented at: 10th ICVG. (Volos, Greece).
Saygaç, S. and Önder, S. (2021). Effects of shoot tip size on in vitro regeneration and virus elimination of grapevine cv. superior seedless. Plant Prot. Bull. 61-3. DOI: 10.16955/bitkorb.877123.
Staudt, G. and Kassemeyer, H.H. (1994). Elimination of Grapevine leafroll associated virus type I in Vitis vinifera cv. Lemberger. Vitis 33, 179-180.
Stellmach, G. (1980). Recherche sur les effets d’une réinfection virale de vignes ayant été libéréé de virus pathogènes sur la sélection sanitaire et spécialement par thérmothérapie. Bul. OIV 53, 179-186.
Stewart, S. and Nassuth, A. (2001). RT-PCR based detection of Rupestris stem pitting associated virus within field-grown grapevines throughout the year. Plant Dis. 85, 617–620.
Suzuki, N., Rivero, R.M., Shulaev, V., Blumwald, E. and Mittler, R. (2014). Abiotic and biotics tress combinations. New Phytol. 203, 32–43. doi:10.1111/nph.12797.
Vişoiu, E. and Teodorescu, Al. (2001). Biotehnologii de producere a materialului săditor viticol (Bucharest, Romania: Ceres Publishing House).
Vondras, A.M., Lerno, L., Massonnet, M., Minio, A., Rowhani, A., Liang, D., Garcia, J., Quiroz, D., Figueroa-Balderas, R., Golino, D.A., Ebeler, S.E., Al Rwahnih, M. and Cantu, D. (2021). Rootstock influences the effect of Grapevine leafroll-associated viruses on berry development and metabolism via abscisic acid signalling. Mol. Plant Pathol. 22(8), 984-1005. doi: 10.1111/mpp.13077.
Walter, B. (1988). Effects of Grapevine fleck virus on some American and French-American hybrid rootstocks. Vitis 27(1), 13–22.
Walter, B. and Martelli, G.P. (1996). Sélection clonele de la vigne: sélection sanitaire et sélection pomologique. Influence des viroses et qualité. 1-ère Partie: Effets des viroses sur la culture de la vigne et ses produits. Bulletin del'O.I.V 789-790, 945-971.
Wang, Q., Mawassi, M., Li, P., Gafny, R., Sela, I. and Tanne, E. (2003). Elimination of Grapevine virus A (GVA) by cryopreser¬vation of in vitro-grown shoot tips of Vitis vinifera L. Plant Sci. 165, 321-327.
Youssef, S.A., Al-Dhaher, M.M.A. and Shalaby, A.A. (2009). Elimination of Grapevine fanleaf virus (GFLV) and Grapevine leaf roll-associated virus-1(GLRaV-1) from infected grapevine plants using meristem tip culture. Int. J. Virol. 5(2), 89-99.
Zherdev, A.V., Vinogradova, S.V., Byzova, N.A., Porotikova, E.V., Kamionskaya, A.M. and Dzantiev, B.B. (2018). Methods for the Diagnosis of Grapevine Viral Infections: A Review. Agriculture 8(12), 195. https://doi.org/10.3390/agriculture8120195.
https://eur-lex.europa.eu/legal-content/RO/TXT/PDF/?uri=CELEX:01968L0193-20050714&from=LV.
https://grapes.extension.org/grapevine-fanleaf-degeneration-disease/.
https://www.dpi.nsw.gov.au/agriculture/horticulture/grapes/publications/grapevine-pinot-gris-virus.
Downloads
Published
Issue
Section
License
Copyright (c) 2025 ROMANIAN JOURNAL OF HORTICULTURE
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
