Abstract
A process-based simulation model for the grapevine-downy mildew pathosystem was developed in order to quantitatively synthesize the literature available and to provide a tool to guide strategic decisions for disease management. The model includes: i) the main processes involved in the disease dual epidemics on leaves and clusters, from inoculum mobilisation to disease multiplication on foliage, and to infection of clusters; and ii) host dynamics, i.e. crop development, growth, and physiological and disease-induced senescence. A numerical evaluation was performed to investigate the response of the model to changes of the main epidemiological parameters, i.e. the basic infection rate corrected for the removals (RcOPT), the duration of latency period (LP), the duration of infectious period (IP), and the rate of primary infections (P). Increasing values of RcOPT and IP, and decreasing values of LP resulted in a faster increase of the epidemic on both foliage and clusters, while decreasing values of P delayed epidemics. The simulated dynamics of epidemics on foliage and clusters conformed to patterns of dual epidemics observed for downy mildew. The model can be useful for investigating the effect of strategic disease management tools such as the use of resistant varieties or to investigate the behaviour of the pathosystem under scenarios of climate change.
Similar content being viewed by others
References
Allorent, D., & Savary, S. (2005). Epidemiological characteristics of angular leaf spot of bean: A systems analysis. European Journal of Plant Pathology, 113(4), 329–341. https://doi.org/10.1007/s10658-005-4038-y.
Allorent, D., Willocquet, L., Sartorato, A., & Savary, S. (2005). Quantifying and modelling the mobilisation of inoculum from diseased leaves and infected defoliated tissues in epidemics of angular leaf spot of bean. European Journal of Plant Pathology, 113(4), 377–394. https://doi.org/10.1007/s10658-005-4269-y.
Avelino, J., Allinne, C., Cerda, R., Willocquet, L., & Savary, S. (2018). Multiple-disease system in coffee: From crop loss assessment to sustainable management. Annual Review of Phytopathology, 56(1), 611–635. https://doi.org/10.1146/annurev-phyto-080417-050117.
Bernizzoni, F., Gatti, M., Civardi, S., & Poni, S. (2009). Long-term performance of Barbera grown under different training systems and within-row vine spacings. American Journal of Enology and Viticulture, 60(3), 339–348.
Blaise, P., Dietrich, R., & Gessler, C. (1999). VINEMILD: An application-oriented model of Plasmopara viticola epidemics on Vitis vinifera. In Wagenmakers, Van der Werf, & Blaise (Eds.), Acta Horticolture ISHS IOBC/WPRS BulletinI (pp. 187–192).
Bove, F. (2018). A modelling framework for grapevine downy mildew epidemics incorporating foliage-cluster relationships and host plant resistance. Università Cattolica del Sacro Cuore, Piacenza, Italy. Retrieved from http://hdl.handle.net/10280/57899
Bove, F., Savary S., Willocquet L., Rossi V. (Submitted). Simulation of potential epidemics of downy mildew of grapevine in different scenarios of disease conduciveness.
Caffi, T., Legler, S. E., Rossi, V., & Poni, S. (2010). Photosynthetic activity in grape leaf tissue with latent, visible and “virtual” downy mildew lesions. In Proceedings of the “6th international workshop on grapevine downy and powdery mildew" (pp. 60–62). Bordeaux: INRA.
Caffi, T., Gilardi, G., Monchiero, M., & Rossi, V. (2013). Production and release of asexual sporangia in Plasmopara viticola. Phytopathology, 103(1), 64–73. https://doi.org/10.1094/PHYTO-04-12-0082-R.
Campbell, C. L., & Madden, L. V. (1990). Introduction to plant disease epidemiology. New York: John Wiley & Sons.
Carisse, O. (2016). Development of grape downy mildew (Plasmopara viticola) under northern viticulture conditions: Influence of fall disease incidence. European Journal of Plant Pathology, 144(4), 773–783. https://doi.org/10.1007/s10658-015-0748-y.
Chellemi, D. O., & Marois, J. J. (1992). Influence of leaf removal, fungicide applications, and fruit maturity on incidence and severity of grape powdery mildew. American Journal of Enology and Viticulture, 43(1), 53 LP – 57. http://www.ajevonline.org/content/43/1/53.abstract
Dagostin, S., Schärer, H. J., Pertot, I., & Tamm, L. (2011). Are there alternatives to copper for controlling grapevine downy mildew in organic viticulture? Crop Protection, 30(7), 776–788. https://doi.org/10.1016/j.cropro.2011.02.031.
Develey-Rivière, M. P., & Galiana, E. (2007). Resistance to pathogens and host developmental stage: A multifaceted relationship within the plant kingdom. New Phytologist, 175(3), 405–416. https://doi.org/10.1111/j.1469-8137.2007.02130.x.
Ellis, M. A., Madden, L. V., & Lalancette, N. (1994). A disease forecasting program for grape downy mildew in Ohio. Special report (New York State Agricultural Experiment Station), 68, 92–95.
Emmett, R. W., Wicks, T. J., & Magarey, P. A. (1992). Downy mildew of grapes. Plant diseases of international importance. Volume III. Diseases of fruit crops. Englewood Cliffs: Prentice Hall.
Farrar, J. F. (1992). Beyond photosynthesis: The translocation and respiration of diseased leaves. In Pests and Pathogens. Plant Responses to Foliar Attack. (Ayres PG,., pp. 102–127). Oxford: Bios Scientific Publishers.
Ficke, A., Gadoury, D. M., & Seem, R. C. (2002). Ontogenic resistance and plant disease management: A case study of grape powdery mildew. Phytopathology, 92(6), 671–675. https://doi.org/10.1094/PHYTO.2002.92.6.671.
Forrester, J. W. (1997). Industrial dynamics. Journal of the Operational Research Society, 48(10), 1037–1041. https://doi.org/10.1057/palgrave.jors.2600946.
Gadoury, D. M. (2015). Climate, asynchronous phenology, ontogenic resistance, and the risk of disease in deciduous fruit crops. In IOBC/WPRS Bulletin (Vol. 110, pp. 15–24).
Gadoury, D. M., Seem, R. C., Ficke, A., & Wilcox, W. F. (2003). Ontogenic resistance to powdery mildew in grape berries. Phytopathology, 93(5), 547–555. https://doi.org/10.1094/PHYTO.2003.93.5.547.
Galet, P. (1977). Les Maladies et les Parasites de la Vigne. Vol 1. Montpellier: Imprimerie du Paysan du Midi.
Gessler, C., & Blaise, P. (1992). An extended progeny/parent ratio model II. Application to experimental data. Journal of Phytopathology, 134(1), 53–62. https://doi.org/10.1111/j.1439-0434.1992.tb01211.x.
Gessler, C., Pertot, I., & Perazzolli, M. (2011). Plasmopara viticola: a review of knowledge on downy mildew of grapevine and effective disease management. Phytopathologia Mediterranea, 50(1), 3–44. http://hdl.handle.net/10449/20124.
Giuntoli, A., & Orlandini, S. (2000). Effects of downy mildew on photosynthesis of grapevine leaves. Acta Horticolture, 526, 461–466.
Gobbin, D., Jermini, M., & Gessler, C. (2003). The genetic underpinning of the minimal fungicide strategy. In Integrated Protection and Production in Viticulture IOBC wprs Bulletin (Vol. 26, pp. 101–104). http://www.iobc-wprs.org/pub/bulletins/iobc-wprs_bulletin_2003_26_08.pdf#page=295
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(4), 522–534. https://doi.org/10.1111/j.1365-3059.2005.01208.x.
Goidanich, G. (1959). Manuale di patologia vegetale - v. 1–4. Bologna (Italy): Edizioni Agricole.
Grünzel, H. (1961). Untersuchungen über die Oosporenbildung beim Falschen Mehltau der Weinrebe (Peronospora viticola de Bary). Zeitschrift für Pflanzenkrankheiten (Pflanzenpathologie) und Pflanzenschutz, 68(2), 65–80 http://www.jstor.org/stable/43231828.
Gutierrez, A. P., Williams, D. W., & Kido, H. (1985). A model of grape growth and development: The mathematical structure and biological considerations. Crop Science, 25(5), 721–728. https://doi.org/10.2135/cropsci1985.0011183x002500050001x.
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). Studies on Plasmopara viticola epidemics in the vineyard. In Atti del Convengo su Modelli Euristici ed Operativi in Agricoltura (pp. 266–273). Caserta (Italy): Societa Italiana di Fitoiatria.
Hill, G. K. (2000). Simulation of P. viticola oospore-maturation with the model SIMPO. Bulletin OILB/SROP, 23(4), 7–8.
Jeger, M. J. (1984). Relating disease progress to cumulative numbers of trapped spores: Apple powdery mildew and scab epidemics in sprayed and unsprayed orchard plots. Plant Pathology, 33(4), 517–523. https://doi.org/10.1111/j.1365-3059.1984.tb02876.x.
Jeger, M. J., Gareth Jones, D., & Griffiths, E. (1983). Components of partial resistance of wheat seedlings to Septoria nodorum. Euphytica, 32(2), 575–584. https://doi.org/10.1007/BF00021470.
Jermini, M., Dietrich, R., Aerni, J., & Blaise, P. (2000). Early control of grapevine downy mildew allows a reduction of fungicide application. In Integrated Control in Viticulture IOBC/WPRS Bulletin 23, 3–6.
Kassemeyer, H. H. (1994). Experience with electronic warning of downy mildew of grapevine. In D. M. Gadoury & R. C. Seem (Eds.), Proc. Int. Workshop Grapevine Downy Mildew Modeling, 1st. (pp. 80–81). N.Y. Agric. Exp. Stn. Spec. Rep. 68.
Kennelly, M. M., Gadoury, D. M., Wilcox, W. F., Magarey, P. A., & Seem, R. C. (2005). Seasonal development of ontogenic resistance to downy mildew in grape berries and rachises. Phytopathology, 95(12), 1445–1452. https://doi.org/10.1094/PHYTO-95-1445.
Kennelly, M. M., Gadoury, D. M., Wilcox, W. F., Magarey, P. A., & Seem, R. C. (2007). Primary infection, lesion productivity, and survival of sporangia in the grapevine downy mildew pathogen Plasmopara viticola. Phytopathology, 97(4), 512–522. https://doi.org/10.1094/PHYTO-97-4-0512.
Kranz, J. (1979). Simulation of epidemics caused by Venturia inaequalis (Cooke) Aderh. EPPO Bulletin, 9(3), 235–242. https://doi.org/10.1007/978-3-642-96220-2_7.
Kranz, J., & Hau, B. (1980). Systems analysis in epidemiology. Annual Review of Phytopathology, 18(1), 67–83. https://doi.org/10.4324/9781315123806.
Lalancette, N., Madden, L. V., & Ellis, M. A. (1988). A quantitative model for describing the sporulation of Plasmopara viticola on grape leaves. Phytopathology, 78(10), 1316–1321. https://doi.org/10.1094/phyto-78-1316.
Leroy, P., Smits, N., Cartolaro, P., Delière, L., Goutouly, J. P., Raynal, M., & Alonso Ugaglia, A. (2013). A bioeconomic model of downy mildew damage on grapevine for evaluation of control strategies. Crop Protection, 53, 58–71. https://doi.org/10.1016/j.cropro.2013.05.024.
Levin, S. A., Grenfell, B., Hastings, A., & Perelson, A. S. (1997). Mathematical and computational challenges in population biology and ecosystems science. Science, 275(5298), 334 LP – 343. https://doi.org/10.1126/science.275.5298.334.
Loomis, R. S., & Adams, S. S. (1983). Integrative analyses of host-pathogen relations. Annual Review of Phytopathology, 21(1), 341–362. https://doi.org/10.1146/annurev.py.21.090183.002013.
Lorenz, D. H., Eichhorn, K. W., Bleiholder, H., Klose, R., Meier, U., & Weber, E. (1995). Growth stages of the grapevine: Phenological growth stages of the grapevine (Vitis vinifera L. ssp. vinifera)—Codes and descriptions according to the extended BBCH scale. Australian Journal of Grape and Wine Research, 1(2), 100–103. https://doi.org/10.1111/j.1755-0238.1995.tb00085.x.
Madden, L. V., Hughes, G., & van den Bosch, F. (2007). The Study of Plant Disease Epidemics. St Paul, MN: American Phytopathological society (APS press). https://doi.org/10.1094/9780890545058.fm.
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(1), 29–33.
Müller, K., & Sleumer, H. (1934). Biologische Untersuchungen über die Peronosporakrankheit des Weinstockes mit besonderer Berücksichtigung ihrer Bekämpfung nach der Inkubationskalendermethode. Landwirtschaftliche Jahrbucher, 79(4), 509–576.
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. EPPO Bulletin, 23(4), 619–626.
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(3), 182–189.
Parlevliet, J. E. (1979). Components of resistance that reduce the rate of epidemic development. Annual Review of Phytopathology, 17(1), 203–222. https://doi.org/10.1146/annurev.py.17.090179.001223.
Poni, S., Palliotti, A., & Bernizzoni, F. (2006). Calibration and evaluation of a STELLA software-based daily CO2 balance model in Vitis vinifera L. Journal of the American Society for Horticultural Science, 131(2), 273–283.
Rabbinge, R., & de Wit, C. T. (1989). Theory of modelling and systems. In Simulation and Systems Management in Crop Protection (pp. 3–15). Wageningen: Centre for Agricultural Publishing and Documentation (Pudoc). https://doi.org/10.1016/0308-521x(93)90084-f.
Reuveni, M. (1998). Relationships between leaf age, peroxidase and β-1, 3-GIucanase activity, and resistance to downy mildew in grapevines. Journal of Phytopathology, 146(10), 525–530.
Rossi, V., & Caffi, T. (2012). The role of rain in dispersal of the primary inoculum of Plasmopara viticola. Phytopathology, 102(2), 158–165. https://doi.org/10.1094/PHYTO-08-11-0223.
Rossi, V., Bugiani, R., Girometta, B., & Giosuè, S. (2002). Funghi, batteri e virus: Influenza delle condizioni metereologiche sulle infezioni primarie di Plasmopara viticola in Emilia Romagna. In A. Brunelli & A. Canova (Eds.), Atti delle Giornate Fitopatologiche (Vol. 2, pp. 1000–1008). Bologna: CLUEB.
Rossi, V., Caffi, T., Giosue, S., Girometta, B., Bugiani, R., Spanna, F., et al. (2005). Elaboration and validation of a dynamic model for primary infections of Plasmopara viticola. Rivista Italiana di Agrometeorologia, 3, 7–13 http://hdl.handle.net/10807/45996.
Rossi, V., Caffi, T., Giosuè, S., & Bugiani, R. (2008). A mechanistic model simulating primary infections of downy mildew in grapevine. Ecological Modelling, 212(3–4), 480–491. https://doi.org/10.1016/j.ecolmodel.2007.10.046.
Rossi, V., Giosuè, S., & Caffi, T. (2009). Modelling the dynamics of infections caused by sexual and asexual spores during Plasmopara Viticola epidemics. Journal of Plant Pathology, 91(3), 615–627.
Rossi, V., Caffi, T., & Gobbin, D. (2013). Contribution of molecular studies to botanical epidemiology and disease modelling: Grapevine downy mildew as a case-study. European Journal of Plant Pathology, 135(4), 641–654. https://doi.org/10.1007/s10658-012-0114-2.
Royle, D. J. (1973). Quantitative relationships between infection by the hop downy mildew pathogen, Pseudoperonospora humuli, and weather and inoculum factors. Annals of Applied Biology, 73(1), 19–30. https://doi.org/10.1111/j.1744-7348.1973.tb01305.x.
Rumbou, A., & Gessler, C. (2004). Genetic dissection of Plasmopara viticola population from a Greek vineyard in two consecutive years. European Journal of Plant Pathology, 110(4), 379–392. https://doi.org/10.1023/B:EJPP.0000021061.38154.22.
Savary, S., & Willocquet, L. (2014). Simulation modeling in botanical epidemiology and crop loss analysis. The Plant Health Instructor. APSnet Education Center. https://doi.org/10.1094/phi-a-2014-0314-01.
Savary, S., De Jong, P. D., Rabbinge, R., & Zadoks, J. C. (1990). Dynamic simulation of groundnut rust: A preliminary model. Agricultural Systems, 32(2), 113–141. https://doi.org/10.1016/0308-521X(90)90034-N.
Savary, S., Delbac, L., Rochas, A., Taisant, G., & Willocquet, L. (2009). Analysis of nonlinear relationships in dual epidemics, and its application to the management of grapevine downy and powdery mildews. Phytopathology, 99(8), 930–942. https://doi.org/10.1094/PHYTO-99-8-0930.
Savary, S., Nelson, A., Willocquet, L., Pangga, I., & Aunario, J. (2012). Modeling and mapping potential epidemics of rice diseases globally. Crop Protection, 34, 6–17. https://doi.org/10.1016/j.cropro.2011.11.009.
Savary, S., Stetkiewicz, S., Brun, F., & Willocquet, L. (2015). Modelling and mapping potential epidemics of wheat diseases—Examples on leaf rust and Septoria tritici blotch using EPIWHEAT. European Journal of Plant Pathology, 142(4), 771–790. https://doi.org/10.1007/s10658-015-0650-7.
Savary, S., Nelson, A. D., Djurle, A., Esker, P. D., Sparks, A., Amorim, L., Bergamin Filho, A., Caffi, T., Castilla, N., Garrett, K., McRoberts, N., Rossi, V., Yuen, J., & Willocquet, L. (2018). Concepts, approaches, and avenues for modelling crop health and crop losses. European Journal of Agronomy, 100(September 2016), 4–18. https://doi.org/10.1016/j.eja.2018.04.003.
Shoemaker, C. A. (1981). Applications of dynamic programming and other optimization methods in Pest management. IEEE Transactions on Automatic Control, 26(5), 1125–1132. https://doi.org/10.1109/TAC.1981.1102782.
Sun, P., & Zeng, S. (1994). On the measurement of the corrected basic infection rate. Zeitschrift fur Pflanzenkrankheiten und Pflanzenschutz, 101(3), 297–302.
Vanderplank, J. E. (1963). Plant diseases: Epidemics and control. Academic Press Inc. (New York).
Wermelinger, B., & Koblet, W. (1990). Seasonal growth and nitrogen distribution in grapevine leaves, shoots and grapes. Vitis, 29(1), 15–26.
Willocquet, L., & Savary, S. (2004). An epidemiological simulation model with three scales of spatial hierarchy. Phytopathology, 94(8), 883–891. https://doi.org/10.1094/PHYTO.2004.94.8.883.
Winkler, A. J., Cook, J. A., Kliewer, W. M., & Lider, L. A. (1974). The physiology of the vine. In General viticulture (pp. 90–109). Berkeley, Calif. (USA): University of California Press.
Zadoks, J. C. (1971). Systems analysis and the dynamics of epidemics. Phytopathology, 61, 600–610.
Zadoks, J. C. (1977). Simulation models of epidemics and their possible use in the study of disease resistance. In Proceedings of a symposium on induced mutations against plant diseases (pp. 109–118). Vienna, Austria: International Atomic Energy Agency (IAEA). http://inis.iaea.org/search/search.aspx?orig_q=RN:09373754
Zadoks, J. C., & Rabbinge, R. (1985). Modelling to a purpose. CA Gilligan (Eds) Advances in Plant Pathology, mathematical Modelling of crop diseases Vol. 3 academic press London 231–244Zadoks, J. C., & Schein, R. D. (1979). Epidemiology and plant disease management. New York, N.Y. (USA) Oxford Univ. press.
Acknowledgments
This study was supported by the Doctoral School on the Agro-Food System (Agrisystem) of the Università Cattolica del Sacro Cuore (Italy).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The Authors declare that the present manuscript complies with the Ethical Rules of good scientific practice applicable for the European Journal of Plant Pathology.
Conflict of interest
The authors declare that they have no conflict of interest. All authors are informed and agree on the publication of the manuscript.
Research involving human participants and/or animals
Not applicable, the research does not involve humans or animals.
Informed consent
Not applicable, the research does not involve human participants.
Rights and permissions
About this article
Cite this article
Bove, F., Savary, S., Willocquet, L. et al. Designing a modelling structure for the grapevine downy mildew pathosystem. Eur J Plant Pathol 157, 251–268 (2020). https://doi.org/10.1007/s10658-020-01974-2
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-020-01974-2