Abstract
While the age-related susceptibility of potatoes to late blight is well-known, the universality of this relationship is unclear. This study aimed at resolving the dilemma of the age-related susceptibility in late blight epidemics by analysing the disease progress curves of three potato cultivars (Folva, Novano and Nofy). The following epidemiological parameters were analysed: incubation period (IP), standardised apparent infection rate (SAIR), inflection point (InflPoint), time to reach 1% severity (T1) and relative area under the disease progress curve (rAUDPC). Cultivar had a pronounced effect on IP. However, neither plant age nor age × cultivar had a significant effect on IP. Overall, cultivar was the most important determinant of susceptibility to late blight. Differences between plant ages for late blight susceptibility were more evident in 2019 compared to 2020. Susceptibility to late blight increased with plant age according to rAUDPC, InflPoint and T1. Based on SAIR, younger (Folva) and middle-aged (Novano) plants were the most susceptible in 2019, whereas no differences were apparent between plant ages in 2020. Based on principal component analysis, the first component (Comp.1) accounted for ~79% (2019) and ~ 81% (2020) compared to ~21% (2019) and ~ 19% (2020) of the second component (Comp.2). Comp. 1 was strongly associated with rAUDPC, InflPoint and T1, thus, the conclusions based on these parameters, i.e. susceptibility increases with plant age, were more likely than with SAIR, which on the other hand was strongly associated with Comp.2. In conclusion, our study showed that the susceptibility of potatoes to late blight increases with plant age.
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Data availability
The datasets generated during this study are available from the corresponding author on reasonable request.
References
Abuley, I. K. & Hansen, H. H. (2020). Control of late blight (Phytophthora infestans) and early blight (Alternaria solani) in potatoes. In: Jørgensen, L.N. Heick, T.M., Abuley, I.K., Mathiassen, S.K., Jensen, P.K., Kristjansen, H.S. & Hartvig, P. (Eds), Applied crop protection 2019. : Aarhus Universitet - DCA - Nationalt Center for Fødevarer og Jordbrug.
Abuley, I. K., Hansen, J. G., & Lassen, P. (2019). Results from the trap nursery network in Europe. In H. T. A. M. Schepers (Ed.), Seventeenth Euroblight workshop. Wageningen University.
Abuley, I. K., Nielsen, B. J., & Labouriau, R. (2018). Resistance status of cultivated potatoes to early blight (Alternaria Solani) in Denmark. Plant Pathology, 67, 315–326.
Andrivon, D., Pellé, R., & Ellissèche, D. (2006). Assessing resistance types and levels to epidemic diseases from the analysis of disease Progress curves: Principles and application to potato late blight. American Journal of Potato Research, 83, 455–461.
Beaumont, A. (1934). On the relation between the stage of development of the potato crop and the incidence of blight (Phytophthora Infestans). Annals of Applied Biology, 21, 23–47.
Breuning-Madsen, H., Nørr, A., & Holst, K. A. (1992). The Danish soil classification: Atlas over Denmark I. The Royal Danish Geographical Society.
Campbell, C. L., Madden, L. V., & Pennypacker, S. P. (1980). Structural characterization of bean root-rot epidemics. Phytopathology, 70, 152–155.
Carnegie, S. F., & Colhoun, J. (1980). Differential leaf susceptibility to Phytophthora infestans on potato plants of cv. King Edward. Journal of Phytopathology, 98, 108–117.
Carnegie, S. F., & Colhoun, J. (1982). Susceptibility of potato leaves to Phytophthora infestans in relation to plant age and leaf position. Journal of Phytopathology, 104, 157–167.
Colon, L. T., Turkensteen, L. J., Prummel, W., Budding, D. J., & Hoogendoorn, J. (1995). Durable resistance to late blight (Phytophthora infestans) in old potato cultivars. European Journal of Plant Pathology, 101, 387–397.
Colquhoun, D. (2019). The false positive risk: A proposal concerning what to do about p-values. The American Statistician, 73, 192–201.
Cooke, D. E. L., Cano, L. M., Raffaele, S., Bain, R. A., Cooke, L. R., Etherington, G. J., Deahl, K. L., Farrer, R. A., Gilroy, E. M., Goss, E. M., Grünwald, N. J., Hein, I., Maclean, D., Mcnicol, J. W., Randall, E., Oliva, R. F., Pel, M. A., Shaw, D. S., Squires, J. N., et al. (2012). Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathog, 8(10), e1002940. https://doi.org/10.1371/journal.ppat.1002940
Corbiere, R., Puidet, B., Mabon, R., Guibert, M., Chatot, C., Saubeau, G., Aurousseau, F., & Dewaegeneire5, P. & Andrivon, D. (2019). Pathogenicity – A driver for the epidemic potential of the clonal lineage EU_41_A2 of Phytophthora infestans inside sexually reproducing populations of Nordic European countries? In H. T. A. M. Schepers (Ed.), Seventeenth Euroblight workshop. Wageningen.
Dorrance, A. E., & Inglis, D. A. (1997). Assessment of greenhouse and laboratory screening methods for evaluating potato foliage for resistance to late blight. Plant Disease, 81, 1206–1213.
Dowley, L. J., Carnegie, S. F., Balandras-Chatot, C., Ellissèche, D., Gans, P., Schöber-Butin, B., & Wustman, R. (1999). Guidelines for evaluating disease resistance in potato cultivars. Foliage blight resistance (field test)Phytophthora infestans (Mont.) de Bary. Potato Research, 42, 107–111.
European Commission. (2020). Factsheet: From farm to fork: Our food, our health, our planet, our future. Retrieved March 17, 2021, from https://ec.europa.eu/commission/presscorner/detail/en/fs_20_908.
Euroblight news. 2020. Results of the EuroBlight potato late blight monitoring in 2019 [online]. Euroblight. Available: https://agro.au.dk/forskning/internationale-platforme/euroblight/currently/news/nyhed/artikel/results-of-the-euroblight-potato-late-blight-monitoring-in-2019/ [Accessed 17-03-2021].
Fry, W. E. (1978). Quantification of general resistance of potato cultivars and fungicide effects for integrated control of potato late blight. Phytopathology, 68, 1650–1655.
Fry, W. E. (2007). The canon of potato science: 10. Late blight and early blight. Potato Research, 50, 243–245.
Fry, W. E. (2020). Phytophthora infestans: The itinerant invader; “late blight”: The persistent disease. Phytoparasitica, 48, 87–94.
Fry, W. E., & Apple, A. E. (1986). Disease management implications of age-related changes in susceptibility of potato foliage to Phytophthora infestans. American Potato Journal, 63, 47–56.
Grainger, J. (1956). Host nutrition and attack by fungal parasites. Phytopathology, 46, 445–456.
Grainger, J. (1968). Disease assessment and the prevention of crop loss. World Crops, 20, 21–28.
Goodman, S. N. (1993). P values, hypothesis tests, and likelihood: Implications for epidemiology of a neglected historical debate. American Journal of Epidemiology, 137, 485–496.
Hansen, J. G., Lassen, P., & Abuley, I. K. (2019). IPM2.0: Test of a DSS including information from a trap nursery. In H. T. a. M. Schepers (Ed.), proceedings of the seventeenth Euroblight workshop (pp. 105-113). Wageningen University. WUR special report no. 19.
Hansen, J. G., & Abuley, I. K. (2020). Nye skimmeltyper i Danmark betyder at vi skal ændre praksis. Magasinet Danske Kartofler. Danske Kartofler.
Hansen, J. G., Colon, L. T., Cooke, D. E. L., Lassen, P., Nielsen, B. J., Cooke, L. R., Andrivon, D., & Lees, A. K. (2007). Eucablight - collating and analysing pathogenicity and resistance data on a European scale. EPPO Bulletin, 37, 383–390.
Kaiser, H. F. (1960). The application of electronic computers to factor analysis. Educational and Psychological Measurement, 20, 141–151.
Kessel, G. J. T., Mullins, E., Evenhuis, A., Stellingwerf, J., Cortes, V. O., Phelan, S., Van Den Bosch, T., Förch, M. G., Goedhart, P., Van Der Voet, H., & Lotz, L. A. P. (2018). Development and validation of IPM strategies for the cultivation of cisgenically modified late blight resistant potato. European Journal of Agronomy, 96, 146–155.
Lees, A. K., Stewart, J. A., Lynott, J. S., Carnegie, S. F., Campbell, H., & Roberts, A. M. I. (2012). The effect of a dominant Phytophthora infestans genotype (13_A2) in Great Britain on host resistance to foliar late blight in commercial potato cultivars. Potato Research, 55, 125–134.
Lenth, R. 2020. Emmeans: Estimated marginal means, aka least-squares means. R package version 1.5.1.
Loegering, W. Q. (1976). Rating general resistance on a single-plant basis. Phytopathology, 66, 1445.
Lowings, P. H., & Garcia Acha, I. (1959). Some factors affecting growth of Phytophthora infestans (mont.) de Bary: I. P. Infestans on living potato leaves. Transactions of the British Mycological Society, 42, 491–501.
Madden, L. V., Hughes, G., & van den Bosch, F. (2007). The Sudy of plant disease epidemics. APS Press.
Pelletier, J. R., & Fry, W. E. (1989). E. Characterization of resistance to early blight in three potato cultivars: Incubation period, lesion expansion rate, and spore production. Phytopathology. Phytopathology, 79, 511–517.
Miljøstyrelsen (1995). Orientering fra Miljøstyrelsen. Bekæmpelsesmiddelstatistik 1994, nr. 8.
Miljøstyrelsen (2021). Behandlingshyppighed og pesticidbelastning baseret på salg og forbrug. Bekæmpelsesmiddel-statistik 2019, nr. 48.
Pinheiro, J., Bates, D., Debroy, S., Sarkar, D. & Team, R. C. (2020). Nlme:Linear and nonlinear mixed effects models. R package version 3.1–148.
Populer, C. (1978). Changes in Host Susceptibility with Time. In: J.G. Horsfall & E.B. Cowling (Eds.), How Disease Develops in Populations. Academic Press (Vol. II, pp239–262).
Core Team, R. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Royall, R. (2000). On the probability of observing misleading statistical evidence. Journal of the American Statistical Association, 95, 760–768.
Schepers, H. T. A. M., Kessel, G. J. T., Lucca, F., Förch, M. G., Van Den Bosch, G. B. M., Topper, C. G., & Evenhuis, A. (2018). Reduced efficacy of fluazinam against Phytophthora infestans in the Netherlands. European Journal of Plant Pathology, 151, 947–960.
Shaner, G., & Finney, R. E. (1977). The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knox wheat. Phytopathology, 77, 1051.
Shibata, Y., Kawakita, K., & Takemoto, D. (2010). Age-related resistance of Nicotiana benthamiana against hemibiotrophic pathogen Phytophthora infestans requires both ethylene- and salicylic acid-mediated signaling pathways. Molecular Plant-Microbe Interactions, 23, 1130–1142.
Singh, B. P., & Bhattacharyya, S. K. (1995). Field resistance to late blight of four indian potato cultivars. Potato Research, 38, 171–178.
Śliwka, J., Świątek, M., Tomczyńska, I., Stefańczyk, E., Chmielarz, M., & Zimnoch-Guzowska, E. (2013). Influence of genetic background and plant age on expression of the potato late blight resistance gene Rpi-phu1 during incompatible interactions with Phytophthora infestans. Plant Pathology, 62, 1072–1080.
Sobkowiak, S., & Śliwka, J. (2018). Phytophthora Infestans: Isolation of pure cultures, storage and inoculum preparation. Plant Breeding and Seed Science, 76, 1–15.
Stewart, H. E. (1990). Effect of plant age and inoculum concentration on expression of major gene resistance to Phytophthora infestans in detached potato leaflets. Mycological Research, 94, 823–826.
Visker, M. H. P. W., Keizer, L. C. P., Budding, D. J., Van Loon, L. C., Colon, L. T., & Struik, P. C. (2003). Leaf position prevails over Plant age and leaf age in reflecting resistance to late blight in potato. Phytopathology, 93, 666–674.
Warren, R. C., King, J. E., & Colhoun, J. (1971). Reaction of potato leaves to infection by Phytophthora infestans in relation to position on the plant. Transactions of the British Mycological Society, 57, 501–514.
Warren, R. C., King, J. E., & Colhoun, J. (1973). Reaction of potato plants to Phytophthora infestans in relation to their carbohydrate content. Transactions of the British Mycological Society, 61, 95–105.
Wasserstein, R. L., & Lazar, N. A. (2016). The ASA statement on p-values: Context, process, and purpose. The American Statistician, 70, 129–133.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag New York.
Zeileis, A., & Hothorn, T. (2002). Diagnostic checking in regression relationships. R News, 2, 7–10.
Acknowledgments
Our sincere thanks go to the Green Development and Demonstration Program (GUDP) in Denmark for funding this experiment as part of the “BlightManager” project. We are grateful for the help we received from Hans Hansen Henning during the field experiments. We also thank Kirsten Jensen for proofreading the manuscript.
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Codes used for the data analysis during this study are available from the corresponding author on reasonable request.
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This research received funding from Green Development and Demonstration Program (GUDP), Denmark.
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Abuley, I.K., Hansen, J.G. An epidemiological analysis of the dilemma of plant age and late blight (Phytophthora infestans) susceptibility in potatoes. Eur J Plant Pathol 161, 645–663 (2021). https://doi.org/10.1007/s10658-021-02350-4
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DOI: https://doi.org/10.1007/s10658-021-02350-4