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Seasonal dynamics and tissue distribution of two major viruses associated with grapevine Leafroll under cool climate condition

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Abstract

Grapevine leafroll-associated virus-2 (GLRaV-2) and GLRaV-3 are both (+) ssRNA viruses of the family Closteroviridae and are involved in grapevine leafroll, the most destructive viral disease affecting the global grape/wine industry. Outbreaks of the disease were recently reported in Canada, causing serious concerns to the grape/wine industry. Reliable, sensitive and timely detection is key to the control of the disease. However, information on their seasonal dynamics and tissue distribution under cool climate conditions has been rather limited. We conducted a two-year comprehensive study to elucidate the temporal variation and spatial distribution of both viruses through symptom monitoring, Western blotting and RT-qPCR. Sampling was done monthly from commercial Cabernet Franc and Chardonnay vines from May to October in 2015 and 2016. Both viral RNA and capsid protein levels in leaves remained low during May and June, steadily increased from late July, and peaked in September or October. Interestingly, young berries collected in June contained high levels of viral RNA for both viruses. As expected, the viral RNA levels of GLRaV-2 detected by RT-qPCR using primers targeting the CP region were much higher than those by using primers targeting the genomic RNA. Surprisingly, virtually the same levels of viral RNA were detected for GLRaV-3 regardless of the targeted genomic regions. To ensure accurate detection of both viruses, we recommend using young berries early in the season and leaves and cambial scrapings from late July to harvest. To our knowledge, this is the first report on the seasonal dynamics and tissue distribution of two major grapevine viruses in Canada.

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References

  • Angelini, E., Aboughanem-Sabanadzovic, N., Dolja, V.V., & Meng, B. (2017). Grapevine leafroll-associated virus 2. Chapter 7 in: Grapevine viruses: Molecular biology, diagnostics and management edited by Meng, B., Martelli, G.P., Golino, D.A., & Fuchs, M. Springer International Publishing AG, Cham, Switzerland, 141–165.

  • Atallah, S. S., Gomez, M. I., Fuchs, M., & Martinson, T. E. (2012). Economic impact of grapevine leafroll disease on Vitis vinifera cv. Cabernet Franc in Finger Lakes Vineyards of New York. American Journal of Enology and Viticulture, 63, 73–79.

    Article  Google Scholar 

  • Beuve, M., Sempe, L., & Lemaire, O. (2007). Sensitive one-step real-time RT-PCR method for detecting Grapevine leafroll-associated virus 2 variants in grapevine. Journal of Virological Methods, 141, 117–124.

    Article  CAS  Google Scholar 

  • Burger, J.T., Maree, H.J., Gouveia, P., & Naidu, R. A. (2017). Grapevine leafroll-associated virus 3. Chapter 8 in: Grapevine viruses: Molecular biology, diagnostics and management edited by Meng, B., Martelli, G.P., Golino, D.A., & Fuchs, M. Springer International Publishing AG, Cham, Switzerland. Pages 167–195.

  • Che, X., Piestun, D., Mawassi, M., Yang, G., Satyanarayana, T., Gowda, S., Dawson, W. O., & Bar-Joseph, M. (2001). 5′ coterminal subgenomic RNAs in Citrus tristeza virus. Virology, 283, 374–381.

    Article  CAS  Google Scholar 

  • Constable, F. E., Connellan, J., Nicholas, P., & Rodoni, B. C. (2012). Comparison of enzyme-linked immunosorbent assays and reverse transcription-polymerase chain reaction for the reliable detection of Australian grapevine viruses in two climates during three growing seasons. Australian Journal of Grape Wine Research, 18, 239–244.

    Article  CAS  Google Scholar 

  • Fiore, N., Prodan, S., & Pino, A. M. (2009). Monitoring grapevine viruses by ELISA and RT-PCR throughout the year. Journal of Plant Pathology, 91, 489–493.

    CAS  Google Scholar 

  • Galiakparov, N., Goszczynski, D. E., Che, X., Batuman, O., Bar-Joseph, M., & Mawassi, M. (2003). Two classes of subgenomic RNA of Grapevine virus A produced by internal controller elements. Virology, 312, 434–448.

    Article  CAS  Google Scholar 

  • Gambino, G., Cuozzo, D., Fasoli, M., Pagliarani, C., Vitali, M., Boccacci, P., Pezzotti, M., & Mannini, F. (2012). Co-evolution between Grapevine rupestris stem pitting-associated virus and Vitis vinifera L. leads to decreased defence responses and increased transcription of genes related to photosynthesis. Journal of Experimental Botany, 63, 5919–5933.

    Article  CAS  Google Scholar 

  • Gamm, M., Heloir, M.-C., Kelloniemi, J., Poinssot, B., Wendehenne, D., & Adrian, M. (2011). Identification of reference genes suitable for qRT-PCR in grapevine and application for the study of the expression of genes involved in pterostilbene synthesis. Molecular Genetics and Genomics, 285, 273–285.

    Article  CAS  Google Scholar 

  • Gowda, S., Satyanarayana, T., Ayllon, M. A., Albiach-Martí, M. R., Mawassi, M., Rabindran, S., et al. (2001). Characterization of the cis-acting elements controlling subgenomic mRNAs of Citrus tristeza virus: production of positive- and negative-stranded 3′-terminal and positive-stranded5′-terminal RNAs. Virology, 286, 134–151.

    Article  CAS  Google Scholar 

  • Gutha, L. R., Casassa, L. F., Harbertson, J. F., & Naidu, R. A. (2010). Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves. BMC Plant Biology, 10, 187–205.

    Article  Google Scholar 

  • Jarugula, S., Gowda, S., Dawson, W. O., & Naidu, R. A. (2010). 3′-co terminal subgenomic RNAs and putative cis-acting elements of Grapevine leafroll-associated virus-3 reveals ‘unique’ features of gene expression. Virology Journal, 7, 180.

    Article  Google Scholar 

  • Ling, K. S., Zhu, H. Y., Petrovic, N., & Gonsalves, D. (2001). Comparative effectiveness of ELISA and RT-PCR for detecting Grapevine leafroll-associated Closterovirus-3 in field samples. American Journal of Enology and Viticulture, 52, 21–27.

    CAS  Google Scholar 

  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods, 25, 402–408.

    Article  CAS  Google Scholar 

  • MacKenzie, D. J., Johnson, R. C., & Warner, C. (1996). Incidence of four important viral pathogens in Canadian vineyards. Plant Disease, 80, 955–958.

    Article  Google Scholar 

  • Maliogka, V. I., Martelli, G. P., Fuchs, M., & Katis, N. I. (2015). Control of viruses infecting grapevine. Advances in Virus Research, 91, 175–227.

    Article  CAS  Google Scholar 

  • Maree, H. J., Gardner, H. F. J., Freeborough, M. J., & Burger, J. T. (2010). Mapping of the 5′ terminal nucleotides of Grapevine leafroll-associated virus-3 sgRNAs. Virus Research, 151, 252–255.

    Article  CAS  Google Scholar 

  • Martelli, G. P. (2017). An overview on grapevine viruses, viroids, and the diseases they cause. Grapevine viruses: Molecular biology, diagnostics and management edited by Meng, B., Martelli, G.P., Golino, D.A., & Fuchs, M. Springer International Publishing AG, Cham, Switzerland. 31–46.

  • Martelli, G. P., Ghanem-Sabanadzovic, N. A., Agranovsky, A., Al Rwahnih, M., Dolja, V. V., Dovas, C. I., et al. (2012). Taxonomic revision of the family Closteroviridae with special reference to the grapevine leafroll-associated members of the genus Ampelovirus and the putative species unassigned to the family. Journal of Plant Pathology, 94, 7–19.

    Google Scholar 

  • Meng, B. & Rowhani, A. (2017). Grapevine rupestris stem pitting-associated virus. Grapevine viruses: Molecular biology, diagnostics and management edited by Meng, B., Martelli, G.P., Golino, D.A., & Fuchs, M. Springer International Publishing AG, Cham, Switzerland. Pages 257–288.

  • Meng, B., Credi, R., Petrovic, N., Tomazic, I., & Gonsalves, D. (2003). Antiserum to recombinant virus coat protein detects Rupestris stem pitting associated virus in grapevines. Plant Disease, 87, 515–522.

    Article  CAS  Google Scholar 

  • Naidu, R. A., Maree, H. J., & Burger, J. T. (2015). Grapevine leafroll disease and associated viruses: a unique pathosystem. Annual Review of Phytopathology, 53, 613–634.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Osman, F., Golino, D., Hodzic, E., & Rowhani, A. (2018). Virus distribution and seasonal changes of grapevine leafroll-associated viruses. American Journal of Enology and Viticulture, 69, 70–76.

    Article  CAS  Google Scholar 

  • Poojari, S., Moreau, D. L., Schmidt, A. M., Inglis, D., McFadden-Smith, W., Usher, K., et al. (2018). Grapevine virus diseases in Canada: Current status and future perspectives. Proceeding of the 19th Congress of ICVG, (p. 68), Santiago, Chile.

  • Reid, K. E., Olsson, N., Schlosser, J., Peng, F., & Lund, S. T. (2006). An optimized grapevine RNA isolation procedure and statisticaldetermination of reference genes for real-time RT-PCR duringberry development. BMC Plant Biology, 6, 27.

    Article  Google Scholar 

  • Rimerman, A. F., & Eyler, R. (2017). The economic impact of the wine and grape industry in Canada. The Wine Business Center. Grape growers Ontario. Year in review. 69th Annual Report. (p.14). http://www.canadianvintners.com/wp content/uploads/2017/06/Canada-Economic-Impact-Report-2015.pdf

  • Teliz, D., Tanne, E., Gonsalves, D., & Zee, F. (1987). Field serological detection of viral antigens associated with grapevine leafroll disease. Plant Disease, 71, 704–709.

    Article  Google Scholar 

  • This, P., Lacombe, T., & Thomas, M. R. (2006). Historical origins and genetic diversity of wine grapes. Trends in Genetics, 22, 511–519.

    Article  CAS  Google Scholar 

  • Tsai, C. W., Daugherty, M. P., & Almeida, R. P. P. (2012). Seasonal dynamics and virus translocation of Grapevine leafroll-associated virus 3 in grapevine cultivars. Plant Pathology, 61, 977–985.

    Article  Google Scholar 

  • Vives, M. C., Galipienso, L., Navarro, L., Moreno, P., & Guerri, J. (2002). Characterization of two kinds of subgenomic RNAs produced by Citrus leaf blotch virus. Virology, 295, 328–336.

    Article  CAS  Google Scholar 

  • Xiao, H., Kim, W. S., & Meng, B. (2015). A highly effective and versatile technology for the isolation of RNAs from grapevines and other woody perennials for use in virus diagnostics. Virology Journal, 12, 1–15.

    Article  Google Scholar 

  • Xiao, H., Shabanian, M., Moore, C., Li, C., & Meng, B. (2018). Survey for major viruses in commercial Vitis vinifera wine grapes in Ontario. Virology Journal, 15, 127.

    Article  Google Scholar 

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Acknowledgements

We thank Mr. A. Pavan and Mr. G. Demarco as well as Cave Spring Cellars for the generosity and support throughout this project. We treasure the friendship we have established through this collaboration.

Funding

This project was funded by the Engage (project # EGP469921 and EGP485347) and Discovery (project RGPIN-2014-05306) grant programs of the Natural Sciences and Engineering Research Council of Canada.

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Authors and Affiliations

  1. Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON, N1G 2W1, Canada

    Mehdi Shabanian, Huogen Xiao & Baozhong Meng

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  1. Mehdi Shabanian
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  2. Huogen Xiao
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  3. Baozhong Meng
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Contributions

Mehdi Shabanian collected the samples, designed and carried out the experiments, wrote the initial drafts of the manuscript, and performed data analysis. Huogen Xiao was involved in project design, sample collection, and reviewed the manuscript. Baozhong Meng was responsible for funding, conceived and designed the project, and revised and finalized the manuscript.

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Correspondence to Mehdi Shabanian or Baozhong Meng.

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Fig. S1

Validation of candidate reference genes for use in the quantification of viral RNAs. The selection of the three candidate reference genes to be validated in this study was based on the literature where they were reported to exhibit the most stable expression. Levels of actin transcript remained unchanged from May to September, followed by ubiquitin and EF1-a. Shown is the average of three technical replicates for each candidate gene for Chardonnay. Identical trends were obtained for Cabernet Franc (not shown). (DOCX 35 kb)

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Shabanian, M., Xiao, H. & Meng, B. Seasonal dynamics and tissue distribution of two major viruses associated with grapevine Leafroll under cool climate condition. Eur J Plant Pathol 158, 1017–1031 (2020). https://doi.org/10.1007/s10658-020-02137-z

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