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Synergy between grapevine vitiviruses and grapevine leafroll viruses

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Abstract

An interactive relationship between vitiviruses and grapevine leafroll viruses was characterized in grapevine. Grapevine viruses A and B (GVA and GVB) were found more frequently in the presence of co-infecting Grapevine leafroll associated viruses (GLRaV-1, −2 or −3) than in their absence. The titers of the vitiviruses in co-infection with leafroll viruses were found to be higher than were their titers in the absence of leafroll virus infection. The occurrence of vitivirus-associated stem-pitting symptoms was correlated with leafroll virus co-infection. Specific pairing associations on the species level were found between different viti- and leafroll virus species: GVB was associated preferentially with GLRaV-2; GVA was associated preferentially with GLRaV-1 and GLRaV-3. In contrast to the increase in vitivirus titer seen with leafroll virus co-infection, the incidence and titer of grapevine leafroll virus appeared to be unaltered by vitivirus co-infection. The potential for a synergistic enhancement of grapevine disease in co-infected vines is discussed.

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References

  • Al Rwahnih, M., Osman, F., Sudarshana, M., Uyemote, J., Minafra, A., Saldarelli, P., Martelli, G., & Rowhani, A. (2012). Detection of grapevine leafroll-associated virus 7 using real time qRT-PCR and conventional RT-PCR. Journal of Virological Methods, 179, 383–389.

    Article  PubMed  CAS  Google Scholar 

  • Arnold, K., Golino, D., Cooper, M., Smith, R., & McRoberts, N. (2015) Interpreting a multi-virus survey and designing and delivering virus sampling protocol for industry-wide benefits. American Society of Enology and Viticulture, National Conference, Portland, Abstracts, p. 67.

  • Bertin, S., Pacifico, D., Cavalieri, V., Marzachì, C., & Bosco, D. (2016a). Transmission of Grapevine virus A and Grapevine leafroll-associated viruses 1 and 3 by Planococcus ficus and Planococcus citri fed on mixed-infected plants. The Annals of Applied Biology. https://doi.org/10.1111/aab.12279

  • Bertin, S., Cavaliere, V., Gribaudo, I., Sacco, D., Marzach, C., & Bosco, D. (2016b). Transmission of grapevine virus a and grapevine leafroll-associated virus 1 and 3 by Heliococcus bohemicus (Hemiptera: Pseudococcidae) nymphs from plants with mixed infections. Journal of Economic Entomology, 109, 1504–1511.

    Article  PubMed  CAS  Google Scholar 

  • Credi, R., & Babini, R. (1997). Effects of virus and virus-like infections on growth, yield, and fruit quality of Albana and Trebbiano Romagnolo grapevines. American Journal of Enology and Viticulture, 48, 7–12.

    Google Scholar 

  • Fazeli, C. F., & Rezaian, A. M. (2000). Nucleotide sequence and organization of ten open reading frames in the genome of grapevine leafroll-associated virus 1and identification of three subgenomic RNAs. The Journal of General Virology, 81, 605–615.

    Article  PubMed  CAS  Google Scholar 

  • Fortusimi, A., Scattini, G., Prati, S., Cinquanta, S., & Belli, G. (1997). Transmission of grapevine leafroll associated virus −1 and grapevine virus a by scale insects. In Proc. 12th meeting of the congress of the international council for the study of virus and virus-like diseases of the grapevine (pp. 121–122). Lisbon.

  • Gambino, G., Angelini, E., & Gribaudo, I. (2010). Field assessment and diagnostic methods for detection of grapevine viruses. In S. Delroth, H. Medrano, E. Or, L. Bavanesco, & S. Grando (Eds.), Methodologies and results in grapevine research, Chapter 14 (pp. 211–228). London: Springer.

    Chapter  Google Scholar 

  • Goheen, A. C. (1989). Virus diseases and grapevine selection. American Journal of Enology and Viticulture, 40, 67–72.

    Google Scholar 

  • Golino, D., Sim, S., & Rowhani, A. (2000). The role of GLRaV-2 and GVB in virus-induced rootstock decline in California grapevines. Phytopathology, 90, s28 (Suppliment).

    Google Scholar 

  • Golino, D., Sim, S., & Rowhani, A. (2003). The role of rootstock genotype in the effect of single and mixed infections of grapevine viruses. In Proceedings of the 14th international congress on virus and virus-like diseases of grapevine (pp. 246–247). Locorotondo.

  • Golino, D., Rowhani, A., Klaassen, V., Sim, S., & Al Rwahnih, M. (2015). Grapevine leafroll associated virus 1 effects on different grapevine rootstocks. In Proceedings of the 18th international congress on virus and virus-like diseases of grapevine (pp. 46–47). Ankara.

  • Goszczynski, D. E., & Jooste, A. E. C. (2003). Shiraz disease is transmitted by the mealybug Planococcus ficus and associated with grapevine virus a. In Extended abstracts of the 14th meeting of the international council for the study of viruses and virus-like diseases of the grapevine. Locorotando.

  • Hommay, G., Komar, V., Lemaire, O., & Herrbach, E. (2008). Grapevine virus a transmission by larvae of Parthenolecanium corni. European Journal of Plant Pathology, 121, 185–188.

    Article  Google Scholar 

  • Hommay, G., Le Maguet, J., Komar, V., Lemaire, O. and Herrbach, E. (2009). Transmission of grapevine leafroll-associated virus-1 and-3 (Ampelovirus) and grapevine virus a (Vitivirus) by natural populations of soft scales and mealybugs in the North-Eastern French vineyard. In Proceedings of the 16th meeting of the international council for the study of virus and virus-like diseases of grapevine (pp. 286–287). Dijon.

  • Komar, V., Vigne, E., Demangeat, G., & Fuchs, M. (2007). Beneficial effect of selective virus elimination on the performance of Vitis vinifera cv. Chardonnay. American Journal of Enology and Viticulture, 58, 202–210.

    Google Scholar 

  • Komar, V., Vigne, E., Demangeat, G., Lemaire, O., & Fuchs, M. (2010). Comparative performance of virus-infected Vitis vinifera cv. Savagnin rose grafted onto three rootstocks. American Journal of Enology and Viticulture, 61, 68–73.

    Google Scholar 

  • Le Maguet, J., Beuve, M., Herrbach, E., & Lemaire, O. (2012). Transmissiion of six ampeloviruses and two vitiviruses to grapevine by Phenacoccus aceris. Phytopathology, 102, 717–723.

    Article  PubMed  Google Scholar 

  • Mannini, F., Rolle, L., & Guidoni, S. (2003). Vineyard management to optimize grape quality in virus-free clones of Vitis vinifera L. Acta Horticulturae, (603), 121–126.

  • Maree, H. J., Almeida, R. P., Bester, R., Chooi, K. M., Cohen, D., et al. (2013). Grapevine leafroll associated virus 3. Frontiers in Microbiology, 4, 82–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martelli, G. P. (1993). Rugose wood complex. In G. P. Martelli (Ed.), Graft-transmissible diseases of grapevines. Handbook for detection and diagnosis (pp. 45–54). Rome: United Nations Food and Agriculture Organization.

    Google Scholar 

  • Martelli, G. P. & Boudon-Padieu, T. (2004). Directory of infectious diseases of grapevine and viruses and virus-like diseases of the grapevine. In Options mediterraneennes: serie B (p. 78). Bari, Bibliographic Report 1998–2004.

  • Monis, J., & Bestwick, R. K. (1997). Serological detection of grapevine-associated closteroviruses in infected grapevine cultivars. Plant Disease, 81, 802–808.

    Article  PubMed  Google Scholar 

  • Namba, S., Boscia, D., Azzam, O., Maixner, M., Hu, J. S., Golino, D., & Gonzalves, D. (1991). Purification and preparation of closterovirus-like particles associated with grapevine corky bark disease. Phytopathology, 81, 964–970.

    Article  Google Scholar 

  • Osman, F., Leutenegger, C., Golino, D., & Rowhani, A. (2008). Comparison of low-density arrays, RT-PCR and real-time TaqMan RT-PCR in detection of grapevine viruses. Journal of Virological Methods, 149, 292–299.

    Article  PubMed  CAS  Google Scholar 

  • Rochow, W. F., & Ross, F. (1955). Virus multiplication in plants doubly infected by potato viruses X and Y. Virology, 1, 10–27.

    Article  PubMed  CAS  Google Scholar 

  • Rowhani, A., Uyemoto, J. K., Golino, D., Daubert, S. D., & Al Rwahnih, M. (2016). Viruses involved in graft-incompatibility and decline. In B. Meng, M. Fuchs, G. Martelli, & D. Golino (Eds.), Grapevine viruses: Molecular biology, diagnostics, and management, Chapter 12 (pp. 289–302). New York: Springer.

    Google Scholar 

  • Saldarelli, P., Castellano, M. A., Harrison, B. D., & Martelli, G. P. (2005). Two grapevine viruses in an ornamental Vitis species from Scotland. Journal of Plant Pathology, 87, 76.

    Google Scholar 

  • Santini, D., Mollo, A., Pacifico, D., Borgogno, E., & Mannini, F. (2011). Ecophysiological and agronomic response of two ‘Nebbiolo’ clones to different leafroll virus infection. South African Journal of Enology and Viticulture, 32, 183–189.

    CAS  Google Scholar 

  • Syller, J. (2012). Facilitative and antagonistic interactions between plant viruses in mixed infections. Molecular Plant Pathology, 13, 204–216.

    Article  PubMed  Google Scholar 

  • Vance, V. B. (1991). Replication of potato virus X RNA is altered in coinfections with potato virus Y. Virology, 182, 486–494.

    Article  PubMed  CAS  Google Scholar 

  • Zorlini, A., Prati, S., Bianco, P. A., & Belli, G. (2006). Transmission of grapevine virus a and grapevine leafroll associated virus −3 by Heliococcus Bohemicus. Journal of Plant Pathology, 88, 325–328.

    Google Scholar 

Download references

Acknowledgements

Funded by the American Vineyard Foundation and by a grant from the California Department of Food and Agriculture Fruit Tree, Nut Tree and Grapevine Improvement Advisory Board, to AR.

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Authors and Affiliations

  1. Department of Plant Pathology, University of California, 1 Shields Avenue, Davis, CA, 95616, USA

    A. Rowhani, Steve Daubert, K. Arnold, M. Al Rwahnih, V. Klaassen, D. Golino & J. K. Uyemoto

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  1. A. Rowhani
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  2. Steve Daubert
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  3. K. Arnold
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  4. M. Al Rwahnih
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  5. V. Klaassen
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  6. D. Golino
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  7. J. K. Uyemoto
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Correspondence to Steve Daubert.

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Rowhani, A., Daubert, S., Arnold, K. et al. Synergy between grapevine vitiviruses and grapevine leafroll viruses. Eur J Plant Pathol 151, 919–925 (2018). https://doi.org/10.1007/s10658-018-1426-7

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