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Bois noir affects the yield and wine quality of Vitis vinifera L. cv. ‘Chardonnay’

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Abstract

The Bois noir (BN) disease induced by ‘Candidatus Phytoplasma solani’ (CPs) is common in European vineyards. Its damage has not been fully investigated, especially with regards to wine attributes. The impact of BN on yield, berry composition and wine characteristics of Vitis vinifera L. cv. ‘Chardonnay’ was therefore comprehensively characterized in a 3-year field experiment in Hungary, Eger winegrowing region. Additionally, the bindweed-related tuf-b1 genotype was identified to be involved in the BN pathosystem in the experimental vineyard. Infection of CPs tuf-b1 genotype resulted in severe yield loss, the average decrease in number of bunches and total yield per vine was 56.7% and 68.4%, respectively. Analyses of wines produced from grapes of BN infected vines revealed decreased alcohol, epicatechin and iron contents; and increased organic acids, titratable acidity, catechin and calcium contents. Sensory evaluation of these wines confirmed unfavourable characteristics, i.e. higher acidity, bitterness, and usually pinkish discolouration. Negative impact on berry composition and wine quality were pronounced in the vintage with favourable weather conditions for grapevine production, whereas the negative effects of BN infection were less prominent, even masked, in the vintages with unfavourable weather (wet and cool). To reduce BN-caused damage, the need for improved preventative and curative measures for BN disease is highlighted.

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References

  • Boudon-Padieu, E. (2003). Grapevine phytoplasmas. First Internet Conference on Phytopathogenic Mollicutes Grapevine phytoplasmas; pp. 57–62. http://www.uniud.it/phytoplasma/conf.html. Accessed 24–29 May 1999.

  • Borgo, M., Pegoraro, G., & Sartori, E. (2016). Susceptibility of grape varieties to ESCA disease. 39th World Congress of Vine and Wine, BIO Web of Conferences 7, 01041.

  • Boss, P., Davies, C., & Robinson, S. P. (1996). Expression of anthocyanin biosynthesis pathway genes in red and white grapes. Plant Molecular Biology, 32, 565–569.

    Article  PubMed  CAS  Google Scholar 

  • Constable, F. E. (2010). Phytoplasma epidemiology: Grapevines as a model. In P. G. Weintraub & P. Jones (Eds.), Phytoplasmas: Genomes, plant hosts and vectors (pp. 188–212). Wallingford: CAB International.

    Google Scholar 

  • Cvrković, T., Jović, J., Mitrović, M., Krstić, O., & Toševski, I. (2013). Experimental and molecular evidence of Reptalus panzeri as a natural vector of bois noir. Plant Pathology, 63, 42–53.

    Article  CAS  Google Scholar 

  • Danet, J. L., Balakishiyeva, G., Cimerman, A., Sauvion, N., Marie-Jeanne, V., Labonne, G., et al. (2011). Multilocus sequence analysis reveals the genetic diversity of European fruit tree phytoplasmas and supports the existence of inter-species recombination. Microbiology, 157, 438–450.

    Article  PubMed  CAS  Google Scholar 

  • EFSA PLH Panel (EFSA panel on plant health) (2014). Scientific Opinion on the pest categorisation of Candidatus Phytoplasma solani. EFSA Journal 2014, 12, (12):3924, 3927.

  • Ember, I., Acs, Z., Salar, P., Danet, J. L., Foissac, X., Kölber, M., et al. (2011). Survey and genetic diversity of phytoplasmas from the 16SrV-C and -D subgroups in Hungary. Bulletin of Insectology, 64, 33–34.

    Google Scholar 

  • Endeshaw, S. T., Murolo, S., Romanazzi, G., & Neri, D. (2012). Effects of bois noir on carbon assimilation, transpiration, stomatal conductance of leaves and yield of grapevine (Vitis vinifera) cv. Chardonnay. Physiologia Plantarum, 145, 286–295.

    Article  PubMed  CAS  Google Scholar 

  • Eveillard, S., Jollard, C., Labroussaa, F., Khalil, D., Perrin, M., Desqué, D., et al. (2016). Contrasting susceptibilities to Flavescence Dorée in Vitis vinifera, rootstocks and wild Vitis species. Frontiers in Plant Science, 7, 1762.

    Article  PubMed  PubMed Central  Google Scholar 

  • Foissac, X., & Maixner, M. (2013). Spread of grapevine phytoplasma diseases. Phytopathogenic Mollicutes, 3, 47–50.

    Article  Google Scholar 

  • Foissac, X., & Wilson, M. R. (2010). Current and future distributions of Phytoplasma. In P. G. Weintraub & P. Jones (Eds.), Phytoplasmas: Genomes, plant hosts and vectors (pp. 309–324). Wallingford: CAB International.

    Google Scholar 

  • Garau, R., Sechi, A., Prota, V. A., & Moro, G. (2007). Productive parameters in chardonnay and Vermentino grapevines infected with “bois noir” and recovered in Sardinia. Bulletin of Insectology, 60, 233–234.

    Google Scholar 

  • Himeno, M., Kitazawa, Y., Yoshida, T., Maejima, K., Yamaji, Y., Oshima, K., et al. (2014). Purple top symptoms are associated with reduction of leaf cell death in phytoplasma-infected plants. Scientific Reports, 4, 4111.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hren, M., Nikolić, P., Rotter, A., Blejec, A., Terrier, N., Ravnikar, M., et al. (2009). “Bois noir” phytoplasma induces significant reprogramming of the leaf transcriptome in the field grown grapevine. BMC Genomics, 10, 460.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hunter, J. J., & Visser, J. H. (1988). The effect of partial defoliation, leaf position and developmental stage of the vine on the photosynthetic activity of Vitis vinifera L. cv. Cabernet sauvignon. South African Journal of Enology and Viticulture, 9, 9–15.

    Google Scholar 

  • Jagoueix-Eveillard, S, Tarendeau, F, Guolter, K, Danet, J.L., Bové, J.M., &Garnier, M. (2001). Catharanthus roseus genes regulated differentially by mollicute infections. Molecular Plant-Microbe Interactions, 14, 225–233.

  • Kortekamp, A. (2006). Expression analysis of defence-related genes in grapevine leaves after inoculation with a host and a non-host pathogen. Plant Physiology and Biochemistry, 44, 58–67.

    Article  PubMed  CAS  Google Scholar 

  • Kosovac, A., Johannesen, J., Krstić, O., Mitrović, M., Cvrković, T., Tosevski, I. et al. (2016). Is Hyalesthes obsoletus a species complex undergoing cryptic speciation? More evidence of host-associated genetic differentiation in Southeast Europe. Mitteilungen Klosterneuburg (Supplement), 66, 24–25.

  • Kriston, É., Krizbai, L., Szabó, G., Bujdoso, B., Orosz, S. Z., Dancsházy, Z. S., et al. (2013). First occurrence of grapevine Falvescence dorée in Hungary. Növényvédelem, 49, 433–438.

    Google Scholar 

  • Kuntzmann, P., Foissac, X., Beccavin, I., Chambin, C., Choloux, S., Coarer, M., et al. (2014). Bois noir de la vigne: synthèse des dernières observations. Phytoma, 679, 31–36.

    Google Scholar 

  • Landi, L., & Romanazzi, G. (2011). Seasonal variation of defense-related gene expression in leaves from bois noir affected and recovered grapevines. Journal of Agricultural and Food Chemistry, 59, 6628–6637.

    Article  PubMed  CAS  Google Scholar 

  • Langer, M. & Maixner, M. (2004). Molecular characterisation of grapevine yellows associated phytoplasmas of the stolbur-group based on RFLP-analysis of non-ribosomal DNA. Vitis, 43, 191–200.

  • Lee, I.-M., Davis, R. E., & Gundersen-Rindal, D. E. (2000). Phytoplasma: Phytopathogenic Mollicutes. Annual Review of Microbiology, 54, 221–255.

    Article  PubMed  CAS  Google Scholar 

  • Lepka, P., Stitt, M., Moll, E., & Seemülleer, E. (1999). Effect of phytoplasma infection on concentration and translocation of carbohydrates and amino acids in periwinkle and tobacco. Physiological and Molecular Plant Pathology, 55, 59–68.

    Article  CAS  Google Scholar 

  • Lutter, M., Clark, A. C., Prenzler, P. D., & Scollary, G. R. (2007). Oxidation of caffeic acid in a wine-like medium: Production of dihydroxybenzaldehyde and its subsequent reactions with (+)-catechin. Food Chemistry, 105, 968–975.

    Article  CAS  Google Scholar 

  • Maixner, M. (1994). Transmission of German grapevine yellows (Vergilbungskrankheit) by the planthopper Hyalesthes obsoletus (Auchenorrhyncha:Cixiidae). Vitis, 33, 103–104.

    Google Scholar 

  • Maixner, M. (2011). Recent advances in Bois noir research. In Abstract book of 2nd BN Workshop (pp. 17–32), Castelbrando Cison di Valmarino Italy. Coop. Libraria Editrice Università di Padova: Padova, Italy.

  • Martelli, P.M., & Boudon-Padieu, E. (2006). Grapevine Yellows: individual diseases. In G.P. Martelli, & E. Boudon-Padieu (Ed.), Directory of infectious diseases of grapevines viruses and virus-like diseases of the grapevine: bibliographic report 1998–2004 (pp. 154–167). Bari: CIHEAM. Options Méditerranéennes: Série B. Etudes et Recherches; n. 55, Bari, Italy.

  • Matus, J.T., Vega, A., Loyola, R., Serrano, C., Cabrera, S., & Arce-Johnson, P. (2008). Phytoplasma and virus detection in commercial plantings of Vitis vinifera cv. Merlot exhibiting premature berry dehydration. Electronic Journal of Biotechnology, 11, 1–10.

  • Musetti, R., Buxa, S. V., De Marco, F., Loschi, A., Polizzotto, R., Kogel, K. H., et al. (2013). Phytoplasma-triggered Ca2+ influx is involved in sieve-tube blockage. Molecular Plant Microbe Interactions e-Xtra, 26, 379–386.

    Article  CAS  Google Scholar 

  • Musetti, R., De Marco, F., Farhan, K., Polizzotto, R., Santi, S., Ermacora, P., et al. (2011). Phloem-specific protein expression patterns in apple and grapevine during phytoplasma infection and recovery. Bulletin of Insectology, 64, 211–212.

    Google Scholar 

  • Musetti, R., Marabottini, R., Badiani, M., Martini, M., Sanità di Toppi, L., & Borselli, S. (2007). On the role of H2O2 in the recovery of grapevine (Vitis vinifera cv. Prosecco) from Flavescence dorée disease. Functional Plant Biology, 34, 750–758.

    Article  CAS  Google Scholar 

  • Musetti, R., Paolacci, A., Ciaffi, M., Tanzarella, O. A., Polizzotto, R., Tubaro, F., et al. (2009). Phloem cytochemical modification and gene expression following the recovery of apple plants from apple proliferation disease. Phytopathology, 100, 390–399.

    Article  CAS  Google Scholar 

  • Panassiti, B., Hartig, F., Breuer, M., & Biedermann, R. (2015). Bayesian inference of environmental and biotic factors determining the occurrence of the grapevine disease ‘bois noir’. Ecosphere, 6, 143.

    Article  Google Scholar 

  • Pavan, F., Mori, N., Bressan, S., & Mutton, P. (2012). Control strategies for grapevine phytoplasma diseases: Factors influencing the profitability of replacing symptomatic plants. Phytopathologia Mediterranea, 51, 11–22.

    Google Scholar 

  • Peel, M. C., Finlayson, B. L., & McMahon, T. A. (2007). Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Sciences, 11, 1633–1644.

    Article  Google Scholar 

  • Pracros, P., Renaudin, J., Eveillard, S., Mouras, A., & Hernould, M. (2006). Tomato flower abnormalities induced by stolbur phytoplasma infection are associated with changes of expression of floral development genes. Molecular Plant-Microbe Interactions, 19, 62–68.

    Article  PubMed  CAS  Google Scholar 

  • Quaglino, F., Zhao, Y., Casati, P., Bulgari, D., Bianco, P. A., Wei, W., et al. (2013). 'Candidatus Phytoplasma solani', a novel taxon associated with stolbur and bois noir related diseases of plants. International Journal of Systematic and Evolutionary Microbiology, 63, 2879–2894.

    Article  PubMed  CAS  Google Scholar 

  • Ribéreau-Gayon, P., Glories, Y., Maujean, A., & Dubourdieu, D. (2006). The Chemistry of Wine Stabilization and Treatments Handbook of Enology, volume 2 (2nd ed.). Chichester: Wiley.

    Book  Google Scholar 

  • Romanazzi, G., Murolo, S., & Feliziani, E. (2013). Effects of an innovative strategy to contain grapevine bois noir: Field treatment with resistance inducers. Phytopathology, 103, 785–791.

    Article  PubMed  CAS  Google Scholar 

  • Rusjan, D., Veberič, R., & Mikulič-Petkovšek, M. (2012). The response of phenolic compounds in grapes of the variety “chardonnay” (Vitis vinifera L.) to the infection by phytoplasma bois noir. European Journal of Plant Pathology, 133, 965–974.

    Article  CAS  Google Scholar 

  • Rusjan, D., & Mikulic-Petkovsek, M. (2015). Phenolic responses in 1-year-old canes of Vitis vinifera cv. Chardonnay induced by grapevine yellows (bois noir). Australian Journal of Grape and Wine Research, 21, 123–134.

    Article  CAS  Google Scholar 

  • Salar, P., Charenton, C., Foissac, X., & Malembic-Maher, S. (2013). Multiplication kinetics of Flavescence dorée phytoplasma in broad bean. Effect of phytoplasma strain and temperature. European Journal of Plant Pathology, 135, 371–381.

    Article  Google Scholar 

  • Santi, S., De Marco, F., Polizzotto, R., Grisan, S., & Musetti, R. (2013). Recovery from stolbur disease in grapevine involves changes in sugar transport and metabolism. Frontiers in Plant Science, 4, 1–12.

    Article  Google Scholar 

  • Schwarz, M., Rodríguez, C., Guillén, D. A., & Barroso, C. G. (2012). Evolution of the colour, antioxidant activity and polyphenols in unusually aged Sherry wines. Food Chemistry, 133, 271–276.

    Article  PubMed  CAS  Google Scholar 

  • Sforza, R., Clair, D., Daire, X., Larrue, J., & Boudon-Padieu, E. (1998). The role of Hyalesthes obsoletus (Hemiptera: Cixiidae) in the occurrence of bois noir of grapevine in France. Journal of Phytopathology, 101, 549–556.

    Article  Google Scholar 

  • Sugio, A., Maclean, A. M., Kingdom, H. N., Grieve, V. M., Manimekalai, R., & Hogenhout, S. A. (2011). Diverse targets of phytoplasma effectors: From plant development to defense against insects. Annual Review of Phytopathology, 49, 175–195.

    Article  PubMed  CAS  Google Scholar 

  • Zahavi, T., Sharon, R., Sapir, G., Mawassi, M., Dafny-Yelin, M., & Naor, V. (2013). The long-term effect of Stolbur phytoplasma on grapevines in the Golan Heights. Australian Journal of Grape and Wine Research, 19, 277–284.

    Article  Google Scholar 

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Acknowledgements

We thank Dr. Szabolcs Villangó and Xenia Pálfi for providing meteorological data, as well as István Patai, Zsolt Pálmai, Tamás Lénárd, and Tamás Vincze for their help in the wine preparation process. We thank our colleagues in the Department of Viticulture and the Department of Oenology; and students Eszter Pájer, Bence Czigány, Dorottya Pál and Norbert Simó, for their help with measurements. We also thank Drs. Mária Kölber, Rita Lózsa, István Fazekas and Prof. Miklós Kállay for their valuable comments and Michael Maixner for tuf reference isolates. This project was funded by the National Research, Development and Innovation Fund of the Hungarian Government (KTIA_AIK_12-1-2013-0001) and partly funded by OTKA Research Grant (ID: 113223).

Funding

This project was funded by the National Research, Development and Innovation Fund of the Hungarian Government (KTIA_AIK_12–1–2013-0001) and partly funded by OTKA Research Grant (ID: 113223).

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Correspondence to György Dénes Bisztray.

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Ember, I., Bodor, P., Zsófi, Z. et al. Bois noir affects the yield and wine quality of Vitis vinifera L. cv. ‘Chardonnay’. Eur J Plant Pathol 152, 185–197 (2018). https://doi.org/10.1007/s10658-018-1462-3

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