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Contribution of molecular studies to botanical epidemiology and disease modelling: grapevine downy mildew as a case-study

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Abstract

After being accidentally introduced from the USA at the end of the 19th century, downy mildew caused by Plasmopara viticola (Berk. et Curt.) Berlese et De Toni became one of the most damaging diseases affecting Vitis vinifera in Europe. Downy mildew causes both direct and indirect losses and can lead to severe reduction of yield. Our understanding of the life cycle and epidemiology of P. viticola has been recently altered by molecular studies that revealed that the overwintering inoculum (i.e., the oospores) does more than initiate disease, as was previously thought. A mechanistic model was developed for predicting the entire chain of processes leading to primary infections, and this primary infection model was linked to other models of secondary infection cycles. The model for primary infections defines the length of the primary inoculum season and a seasonal oospore dose consisting of several cohorts of oospores that progressively mature. The model was evaluated by means of Bayesian analysis in both Italy and eastern Canada, and showed high sensitivity, specificity, and accuracy both for potted plants and vineyards. Fungicide applications are necessary to control downy mildew because preventive agronomic practices are not very effective, including host resistance. The use of warning systems based on weather-driven models leads to a reduction in the use and cost of chemicals and a reduction in their environmental impact.

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References

  • Arens, K. (1929). Untersuchungen über Keimung und Zytologie der Oosporen von Plasmopara viticola (Berl. et De Toni). Jahrbucher Wissenschaftliche Botanik, 70, 57–92.

    Google Scholar 

  • Baldacci, E. (1947). Epifitie di Plasmopara viticola (1941–46) nell’Oltrepó Pavese ed adozione del calendario di incubazione come strumento di lotta. Atti Istituto Botanico, Laboratorio Crittogamico, 8, 45–85.

    Google Scholar 

  • Berlese, A. N. (1898). Cytological studies on the fungi. The division of the nucleus and formation of conidia in Oidium. Rivista di Patologia Vegetale, 6, 66–75.

    Google Scholar 

  • Blaise, P., & Gessler, C. (1992). Vinemild: toward a management tool for grape downy mildew. Acta Horticulturae, 313, 257–262.

    Google Scholar 

  • Blaeser, M. (1978). Untersuchungen zur Epidemiologie des falschen Mehltaus an Weinrebe, Plasmopara viticola (Berk. et de Toni). PhD Thesis, Universität Bonn Germany, 127 pp. Tipo di documento non previsto nelle istruzioni della rivista

  • Blaeser, M., & Weltzien, H. C. (1978). The importance of sporulation, dispersal, and germination of sporangia of Plasmopara viticola. Journal of Plant Disease and Protection, 3, 155–161.

    Google Scholar 

  • Blaeser, M., & Weltzien, H. C. (1979). Epidemiologische Studien an Plasmopara viticola zur Verbesserung der Spritzterminbestimmung. Z Pflanzenk Pflanzen, 86, 489–98.

    Google Scholar 

  • Borgo, M., Bellotto, D., & Zanzotto, A. (2004). Composti a base di fenamidone contro la peronospora della vite. L’informatore Agrario, 50, 49–53.

    Google Scholar 

  • Bortolotti, P. P., Nannini, R., & Bugiani, R. (2012). Applicazioni di campo del modello previsionale per peronospora della vite (Plasmopara viticola). In Atti Giornate Fitopatologiche, 2, 401–404.

    Google Scholar 

  • Brooke, P. J. (1979). Effect of light on sporulation of Plasmopara viticola. New Zealand Journal of Botany, 17, 135–138.

    Article  Google Scholar 

  • Burruano, S., Conigliaro, G., & Ciofalo, G. (1992). Indagine preliminare sull’influenza dell’umidità del terreno sulla maturazione delle oospore di Plasmopara viticola. Phytopathologia Mediterranea, 31, 1–4.

    Google Scholar 

  • Burruano, S., Strazzeri, S., & Laviola, C. (1987). Influenza dell’acqua sulla germinazione delle oospore di Plasmopara viticola. Phytopathologia Mediterranea, 26, 19–22.

    Google Scholar 

  • Caffi, T., Rossi, V., Giosuè, S., & Poni, S. (2006). Effect of downy mildew infection on grape leaf photosynthesis. Journal of Plant Pathology, 88(3), 34.

    Google Scholar 

  • Caffi, T., Rossi, V., Cossu, A., & Fronteddu, F. (2007). Empirical vs. mechanistic models for primary infections of Plasmopara viticola. Bulletin OEPP/EPPO Bulletin, 37, 261–271.

    Google Scholar 

  • Caffi, T., & Rossi, V. (2009). L’evoluzione dei modelli epidemiologici per le infezioni primarie di Plasmopara viticola: dalla regola dei ‘3–10’ ai modelli meccanicistici. In M. Severini & S. Pesolillo (Eds.), Modelli per la difesa delle Piante (pp. 59–80). Roma: Aracne Editrice srl.

    Google Scholar 

  • Caffi, T., Rossi, V., Bugiani, R., Spanna, F., Flamini, L., Cossu, A., & Nigro, C. (2009). A model predicting primary infections of Plasmopara viticola in different grapevine-growing areas of Italy. Journal of Plant Pathology, 91(3), 535–548.

    Google Scholar 

  • Caffi, T., Rossi, V., & Bugiani, R. (2010). Evaluation of a warning system for controlling primary infections of grapevine downy mildew. Plant Disease, 94, 709–716.

    Article  CAS  Google Scholar 

  • Caffi, T., Rossi, V., & Lusitani, M. (2011). Long-term survival of Plasmopara viticola oospores. IOBC/WPRS Bulletin, 66, 111–114.

    Google Scholar 

  • Caffi, T., Rossi, V., & Carisse, O. (2011). Evaluation of a dynamic model for primary infections caused by Plasmopara viticola on grapevine in Quebec. Plant Health Progress. doi:10.1094/PHP-2011-0126-01-RS.

  • Caffi, T., Salinari, F., & Rossi, V. (2011). A decision support system for management of organic vineyards against downy mildew. Phytopathology, 101(6), S24.

    Google Scholar 

  • Caffi,T., Gilardi, G., Monchiero, M. & Rossi, V. (2012). Production and dispersal of the asexual sporangia of Plasmopara viticola. Phytopathology, accepted for publication, http://dx.doi.org/10.1094/PHYTO-04-12-0082-R

  • Delmotte, F., Chen, W. J., Richard-Cervera, S., Greif, C., Papura, D., Giresse, X., Mondor-Genson, G., & Corio-Costet, M. F. (2006). Microsatellite DNA markers for Plasmopara viticola, the causal agent of downy mildew of grapes. Molecular Ecology Notes, 6, 379–381.

    Article  CAS  Google Scholar 

  • Develey-Rivière, M. P., & Galiana, E. (2007). Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. New Phytologist, 175, 405–416.

    Article  PubMed  Google Scholar 

  • Dick, M. W. (2002). Towards and understanding of the evolution of the downy mildews. In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.), Advances in downy mildew research (pp. 1–57). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Egger, E., Marinelli, E., & Greco, G. (1994). Un nuovo modello gestionale per il controllo della Peronospora della vite: prime verifiche nell’ambiente viticolo aretino. Rivista di Viticoltura e di Enologia, 47(1), 15–32.

    Google Scholar 

  • Galbiati, C., & Longhin, G. (1984). Indagini sulla formazione e sulla germinazione delle oospore di Plasmopara viticola. Rivista di Patologia Vegetale, 20, 66–80.

    Google Scholar 

  • Galet, P. (1977). Les Maladies et les Parasites de la Vigne. Tome I, Le MaladiesDue à des Végétaux. Montpellier: Le Paysan du. Midi.

  • Gehmann, K. (1987). Untersuchungen zur Epidemiologie und Bekämpfung des Falschen Mehltaus der Weinrebe, verursacht durch Plasmopara viticola. [German]. PhD thesis, University of Stuttgart-Hohenheim.

  • Gessler, C., Rumbou, A., Gobbin, D., Loskill, B., Pertot, I., Raynal, M., & Jermini, M. (2003). A change in our conception of the life cycle of Plasmopara viticola: Oosporic infections versus asexual reproduction in epidemics. IOBC/WPRS Bulletin, 26, 13–16.

    Google Scholar 

  • Gessler, C., Pertot, I., & Perrazzolli, M. (2011). Plasmopara viticola: A review of knowledge on downy mildew of grapevine and effective disease management. Phytopathologia Mediterranea, 50, 3–44.

    Google Scholar 

  • Gobbin, D., Jermini, M., Loskill, B., Pertot, I., Raynal, M., & Gessler, C. (2005). Importance of secondary inoculum of Plasmopara viticola to epidemics of grapevine downy mildew. Plant Pathology, 54, 522–34.

    Article  Google Scholar 

  • Gobbin, D., Pertot, I., & Gessler, C. (2003a). Identification of microsatellite markers for Plasmopara viticola and establishment of high throughput method for SSR analysis. European Journal of Plant Pathology, 109, 153–64.

    Article  CAS  Google Scholar 

  • Gobbin, D., Pertot, I., & Gessler, C. (2003b). Genetic structure of a Plasmopara viticola population in an isolated Italian mountain vineyard. Journal of Phytopathology, 151, 636–646.

    Article  CAS  Google Scholar 

  • Gobbin, D., Rumbou, A., Linde, C. C., & Gessler, C. (2006). Population genetic structure of Plasmopara viticola after 125 years of colonization in European vineyards. Molecular Plant Pathology, 7, 519–531.

    Article  PubMed  CAS  Google Scholar 

  • Goidanich, G., Casarini, B., & Foschi, S. (1957). Lotta antiperonosporica e calendario d’incubazione. Giornale di Agricoltura, 13, 11–14. gennaio.

    Google Scholar 

  • Gregory, C.T. (1915). Studies on Plasmopara viticola. (Official report of the session of Internation Congress of Viticulture, P.P.I.E. San Francisco).

  • Hill, G.K. (1989). Effect of temperature on sporulation efficiency of oilspots caused by Plasmopoara viticola (Berk. & Curt. ex De Bary) Berl. & De Toni in the vineyard. Viticultural and Enological Sciences, 44, 86–90.

  • Hill, G. K. (1990). Plasmopara Risk Oppenheim—a deterministic computer model for the viticultural extension service. Notiziario sulle Malattie delle Piante, 111, 231–223.

    Google Scholar 

  • Hill, G. K., & Breth, K. (1997). Severe primary infections of Plasmopara viticola—A plant pathologists nightmare. Viticulture and. Enological Science, 52, 150–151. Non trovo la rivista per confermarne con sicurezza il titolo esteso!.

    Google Scholar 

  • Hill, G. K. (2000). Simulation of P. viticola oospore-maturation with the model SIMPO. IOBC/WPRS Bulletin, 23(4), 7–8.

    Google Scholar 

  • Istvantti, G., & Palinkas, G. (1913). Etudes sur le mildiou de la vigne. Annales de l’Institut Central Ampelologique Royal Hongrois, 4, 1–125.

    Google Scholar 

  • Jermini, M., Gobbin, D., Blaise, P., & Gessler, C. (2003). Influence of the overwintering methods on the germination dynamic of downy mildew (Plasmopara viticola) oospores. IOBC/WPRS Bulletin, 26, 37–42.

    Google Scholar 

  • Kennelly, M. M., Gadoury, D. M., Wilcox, W. F., Magarey, P., & Seem, R. C. (2005). Seasonal development of ontogenic resistance to downy mildew in grape berries and rachises. Phytopathology, 95(12), 1445–1452.

    Article  PubMed  Google Scholar 

  • Kiefer, B., Riemann, M., Buche, C., Kassemeyer, H.-H., & Nick, P. (2002). The host guides morphogenesis and stomatal targeting in the grapevine pathogen Plasmopara viticola. Planta, 215, 387–393.

    Article  PubMed  CAS  Google Scholar 

  • Lafon, R., & Clerjeau, M. (1988). Downy mildew. In R. C. Pearson & A. C. Goheen (Eds.), Compendium of grape diseases (pp. 11–13). St. Paul: APS Press.

    Google Scholar 

  • Lalancette, N., Ellis, M. A., & Madden, L. V. (1988a). A quantitative model for describing the sporulation of Plasmopara viticola on grape leaves. Phytopathology, 78, 1316–1321.

    Article  Google Scholar 

  • Lalancette, N., Ellis, M. A., & Madden, L. V. (1988b). Development of an infection efficiency model of Plasmopara viticola on American grape based on temperature and duration of leaf wetness. Phytopathology, 78, 794–800.

    Article  Google Scholar 

  • Laviola, C., Burruano, S., & Strazzeri, S. (1986). Influenza della temperatura sulla germinazione delle oospore di Plasmopara viticola (Berk. et Curt.) Berl. et De Toni. Phytopathologia Mediterranea, 25, 80–84.

    Google Scholar 

  • Leu, L. S., & Wu, H. G. (1982). Inoculation, sporulation and sporangial germination of grape downy mildew fungus, Plasmopara viticola. Plant Protection Bulletin (Taiwan), 24, 161–170.

    Google Scholar 

  • Madden, L. V. (2006). Botanical epidemiology: some key advances and its continuing role in disease management. European Journal of Plant Pathology, 11, 3–23.

    Article  Google Scholar 

  • Madden, L. V., Hughes, G., & Ellis, M. A. (1995). Spatial heterogeneity of the incidence of grape downy mildew. Phytopathology, 85, 269–275.

    Article  Google Scholar 

  • Magarey, P. A., Wachtel, M. F., Weir, P. C., & Seem, R. C. (1991). A computer-based simulator for rationale management of grapevine downy mildew Plasmopara viticola. Australian Plant Protection Quarterly, 6, 29–33.

    Google Scholar 

  • Magnien, C., Jacquin, D., Muckensturm, N., & Guillemard, P. (1991). MILVIT: a descriptive quantitative model for the asexual phase of grapevine downy mildew. IOBC/WPRS Bulletin, 21, 451–459.

    Google Scholar 

  • Mariani, L., Failla, O., Dal Monte, G., & Facchinetti, D. (2007). IPHEN: A model for real time production of grapevine phenological maps. Zaragoza: Paper presented at Congress on Climate and Viticulture.

    Google Scholar 

  • Monchiero, M., Gilardi, G., Garibaldi, A., & Gullino, M. L. (2005). Risultati di prove di lotta alla peronospora della vite in Piemonte. Informatore Fitopatologico, 55(4), 32–37.

    Google Scholar 

  • Morroni, M., Zanzotto, A., Caffi, T., & Trevisol, F. (2012). Gestione dei trattamenti antiperonosporici mediante l’ausilio di un modello previsionale sulle infezioni primarie: due annate di sperimentazione nel trevigiano. In ATTI Giornate Fitopatologiche, 2, 393–399.

    Google Scholar 

  • Muller, K., & Sleumer, H. (1934). Biologische Unterschungen über die Peronosorakrankheit des Weinstokes mit besonderer Breücksichtingung threr Bekämpfung nach der Inkhationskalendermethode. Landwirtschaftliche Jahrbucher, 79, 509–576.

    Google Scholar 

  • Orlandini, S., Gozzini, B., Rosa, M., Egger, E., Storchi, P., Maracchi, G., & Miglietta, F. (1993). PLASMO: a simulation model for control of Plasmopara viticola on grapevine. IOBC/WPRS Bulletin, 23, 619–626.

    Google Scholar 

  • Orlandini, S., Massetti, L., & Dalla Marta, A. (2008). An agrometeorological approach for the simulation of Plasmopara viticola. Computers and Electronics in Agriculture, 64(2), 149–161.

    Article  Google Scholar 

  • Ortega-Farías, S. O., Lozano, P., Moreno, Y., & León, L. (2002). Desarrollo de modelos predictivos de fenologìa y evoluciòn de nadurez en vid para vino cv. Cabernet Sauvignon y Chardonnay. Agricultura Técnica, 62, 27–37.

    Google Scholar 

  • Park, E. W., Seem, R. C., Gadoury, D. M., & Pearson, R. C. (1997). DMCAST: a prediction model for grape downy mildew development. Viticultural and Enological Science, 52, 182–189.

    Google Scholar 

  • Ravaz, L. (1914), Traité général de viticulture. III partie: le mildiou. Broché, Montpellier, Paris 14, pp. 282–322.

  • Rho, G., Sancassani, G. P., Toffolatti, S., Fremiot, P., & Vercesi, A. (2004). Further investigations on the length of the incubation period of Plasmopara viticola (Berk. et Curt.) Berl. et De Toni. Atti Giornate Fitopatologiche, 2, 135–142.

    Google Scholar 

  • Richards, C. E. (1959). A flexible growth function for empirical use. Journal of Experimental Botany, 10, 290–300.

    Google Scholar 

  • Ronzon, T. M. S. C. & Clerjeau, M. (1989). Influence of climatic conditions in the autumn on the maturation of oospores of Plasmopara viticola oospores and the degree of attack of mildew in the spring: models of the phenomenon. Proceedings of a meeting of EC Experts’ Group, Thessaloniki, Greece 6–8 October, 1987; 237–243.

  • Rossi, V., Ponti, I., & Cravedi, P. (2000). The status of warning services for plant pests in Italy. IOBC/WPRS Bulletin, 30, 19–29.

    Google Scholar 

  • Rossi, V., Giosuè, S., Girometta, B., & Bugiani, R. (2002). Influenza delle condizioni meteorologiche sulle infezioni primarie di Plasmopara viticola in Emilia-Romagna. Atti Giornate Fitopatologiche, 2, 263–270.

    Google Scholar 

  • Rossi, V., & Caffi, T. (2007). Effect of water on germination of Plasmopara viticola oospores. Plant Pathology, 56(6), 957–966.

    Article  Google Scholar 

  • Rossi, V., Caffi, T., Bugiani, R., Spanna, F., & Della Valle, D. (2008). Estimating the germination dynamics of Plasmopara viticola oospores using hydro-thermal time. Plant Pathology, 57(2), 216–226.

    Article  Google Scholar 

  • Rossi, V., Caffi, T., Giosuè, S., & Bugiani, R. (2008). A mechanistic model simulating primary infections of downy mildew in grapevine. Ecological Modeling, 212(3–4), 480–491.

    Article  Google Scholar 

  • Rossi, V., Giosuè, S., & Caffi, T. (2009). Modelling the dynamics of sexual and asexual spores during Plasmopara viticola epidemics. Journal of Plant Pathology, 91(3), 615–627.

    Google Scholar 

  • Rossi, V., Giosuè, S., & Caffi, T. (2010). Modelling Plant diseases for decision making in crop protection. In E. C. Oerke, R. Gerhards, G. Menz, & R. A. Sikora (Eds.), Precision crop protection—The challenge and use of heterogeneity (p. 441). Dordrecht: Springer.

    Google Scholar 

  • Rossi, V., & Caffi, T. (2012). The role of rain in dispersal of the primary inoculum of Plasmopara viticola. Phytopathology, 102(2), 158–165.

    Article  PubMed  Google Scholar 

  • Rossman, A. Y., & Palm, M. E. (2006). Why aren’t Phytophthora and other Oomycota true Fungi? Outlooks in Pest Management, 17, 217–219.

    Article  Google Scholar 

  • Rumbou, A., & Gessler, C. (2004). Genetic dissection of a Plasmopara viticola population from a Greek vineyard in two consecutive years. European Journal of Plant Pathology, 110, 379–392.

    Article  CAS  Google Scholar 

  • Rumbou, A., & Gessler, C. (2006). Particular structure of Plasmopara viticola populations evolved under Greek island conditions. Phytopathology, 96, 501–509.

    Article  PubMed  Google Scholar 

  • Rumbolz, J., Wirtz, S., Kassemeyer, H. H., Guggenheim, R., Schafer, E., & Buche, C. (2002). Sporulation of Plasmopara viticola: differentiation and light regulation. Plant Biology, 4, 413–422.

    Article  Google Scholar 

  • Salinari, F., Giosue, S., Tubiello, F. N., Rettori, A., Rossi, V., Spanna, F., Rosenzweig, C., & Gullino, M. L. (2006). Downy mildew (Plasmopara viticola) epidemics on grapevine under climate change. Global Change Biology, 12, 1299–1307.

    Article  Google Scholar 

  • Salinari, F., Caffi, T., Legler, S.E. & Rossi, V. (2012). Implementation of epidemiological models for downy and powdery mildew in a DSS for integrated vineyard management. 1–5 October 2012: 10th EFPP (European Foundation for Plant Pathology) conference—“IPM2.0” towards future-proof crop protection in Europe, Wageningen (The Netherlands).

  • Seem, R. C., Magarey, P. A., McCloud, P. I., & Wachtel, M. F. (1985). A sampling procedure to detect grapevine downy mildew. Phytopathology, 75, 1252–1257.

    Article  Google Scholar 

  • Serra, S., Borgo, M., & Canotto, A. (1998). Primary infection occurrence in grapevine downy mildew. IOBC/WPRS Bulletin, 21(2), 5–7.

    Google Scholar 

  • Schweizer, M. & Oliver, R.P. (1999). Molecular Fungal Biology. Cambridge University Press

  • Stryzik, S. (1983). Modèle d’état potentiel d’infection: Application a Plasmopara viticola. Association de Coordination Technique Agricole, Maison Nationale des Eleveurs, 1–46.

  • Tran Manh Sung, C., Strizyk, C., & Clerjeau, M. (1990). Simulation of the date of maturity of Plasmopara viticola oospores to predict the severity of primary infections in grapevine. Plant Disease, 74, 120–124.

    Article  Google Scholar 

  • Unger, S., Büche, C., Boso, S., & Kassemeyer, H.-H. (2007). The course of the colonization of two different Vitis genotypes by Plasmopara viticola indicates compatible and incompatible host–pathogen interactions. Phytopathology, 97, 780–786.

    Article  PubMed  Google Scholar 

  • Vercesi, A., Toffolatti, S. L., Zocchi, G., Guglielmann, R., & Ironi, L. (2010). A new approach to modelling the dynamics of oospore germination in Plasmopara viticola. European Journal of Plant Pathology, 128(1), 113–126.

    Article  Google Scholar 

  • Vercesi, A., Tornaghi, R., Sant, S., Burruano, S., & Faoro, F. (1999). A cytological and ultrastructural study on the maturation and germination of oospores of Plasmopara viticola from overwintering vine leaves. Mycological Research, 103, 193–202.

    Article  Google Scholar 

  • Vercesi, A., Zerbetto, F., & Rho, G. (1999). Impiego dei modelli EPI e PRO nella difesa antiperonosporica del vigneto. Frustula entomologica, 22, 92–97.

    Google Scholar 

  • Vercesi, A., & Liberati, D. (2001). Modelli epidemici: possibilità applicative e prospettive. Informatore Fitopatologico, 51(4), 13–18.

    Google Scholar 

  • Viennot-Bourgin, G. (1949). Les champignons parasites des plantes cultivées. Paris: Masson.

    Google Scholar 

  • Wong, F. P., Burr, H. N., & Wilcox, W. F. (2001). Heterotallism in Plasmopara viticola. Plant Pathology, 50, 427–432.

    Article  Google Scholar 

  • Yarwood, C. E. (1937). The relation of light to the diurnal cycle of sporulation of certain downy mildews. Journal of Agricultural Research, 54, 365–373.

    Google Scholar 

  • Zachos, D. G. (1959). Recherches sur la biologie et l’épidémiologie du mildiou de la Vigne en Grèce. Bases de prévisions et d‘avertissements. Annales de l’Institut Phytopathologique Benaki, 2, 193–355.

    Google Scholar 

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Rossi, V., Caffi, T. & Gobbin, D. Contribution of molecular studies to botanical epidemiology and disease modelling: grapevine downy mildew as a case-study. Eur J Plant Pathol 135, 641–654 (2013). https://doi.org/10.1007/s10658-012-0114-2

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