Simulating crop-disease interactions in agricultural landscapes to analyse the effectiveness of host resistance in disease control: The case of potato late blight

Disease-resistant potato varieties can play a key role in sustainable control of potato late blight. However, when these varieties are more widely used, resistance breakdown can occur as a result of pathogen adaptation. Here we focussed on potato cultivation in the Netherlands, where new (single gene) resistant varieties have been introduced over the last ten years. This new generation of late blight resistant varieties has moderate yield levels and does not meet all market requirements. As a result, adoption rates for resistant varieties have been low so far. We developed a spatially explicit agent-based model to simulate potato production, disease spread and pathogen evolution at the landscape level. We analysed how late blight severity, resistance durability and potato yield are affected by the spatial deployment of a resistant variety, with a lower potential yield than susceptible varieties. The model was applied to an agricultural region in the Netherlands (596 km2) and was run for a period of 36 years using daily weather data as input for crop growth and disease dynamics. The short- and long-term effects of the deployment of a resistant variety were analysed with the model. With respect to short-term dynamics, years were analysed independently to study between year variation. The model demonstrated that in most years, susceptible fields without fungicide application suffered severe yield losses and resistant fields performed better despite their lower potential yield. Resistance breakdown was observed in a small fraction of fields with the resistant variety, but this did not affect mean potato yield or disease incidence in the short term since it occurred at the end of the growing season. Increasing the fraction of potato fields with the resistant variety strongly reduced late blight infection within a landscape. With respect to the long-term effects, the model showed the emergence and spread of a virulent strain over time. The virulent strain gradually took over the pathogen population, decreasing mean potato yields from fields with the resistant variety. This occurred in all landscape compositions where the resistant variety was deployed to different extents. It was found that low as well as high proportions of fields with the resistant variety could increase durability of resistance. With these findings, the model provided more insight into the opportunities and risks related to the use of plant resistance in disease control, an important and sustainable disease management strategy.

[1]  H H Flor,et al.  Current Status of the Gene-For-Gene Concept , 1971 .

[2]  L. Mailleret,et al.  Durable strategies to deploy plant resistance in agricultural landscapes. , 2012, The New phytologist.

[3]  W. Rossing,et al.  Scenario approach for assessing the utility of dispersal information in decision support for aerially spread plant pathogens, applied to Phytophthora infestans. , 2009, Phytopathology.

[4]  F. J. Richards A Flexible Growth Function for Empirical Use , 1959 .

[5]  P. Raatjes,et al.  Monotoring Primary Sources of Inoculum of Phytophthora infestans in The netherlands 1999-2005 , 2007 .

[6]  G. Nigel Gilbert,et al.  Agent-Based Models , 2007 .

[7]  A. Drenth Molecular genetic evidence for a new sexually reproducing population of Phytophthora infestans in Europe , 1994 .

[8]  D. Hamby A review of techniques for parameter sensitivity analysis of environmental models , 1994, Environmental monitoring and assessment.

[9]  A. Holtslag,et al.  Development and validation of a quasi-Gaussian plume model for the transport of botanical spores , 2008 .

[10]  R. Rabbinge,et al.  Ability of the Gaussian plume model to predict and describe spore dispersal over a potato crop , 2002 .

[11]  W. Fry,et al.  Phytophthora infestans: the plant (and R gene) destroyer. , 2008, Molecular plant pathology.

[12]  Jean-Noël Aubertot,et al.  SIPPOM-WOSR: A Simulator for Integrated Pathogen POpulation Management of phoma stem canker on Winter OilSeed Rape I. Description of the model , 2010 .

[13]  Didier Andrivon,et al.  Fitness costs associated with unnecessary virulence factors and life history traits: evolutionary insights from the potato late blight pathogen Phytophthora infestans , 2010, BMC Evolutionary Biology.

[14]  S. B. Goodwin,et al.  Rapid evolution of pathogenicity within clonal lineages of the potato late blight disease fungus , 1995 .

[15]  W. Werf,et al.  Multi-scale modeling of potato late blight epidemics , 2008 .

[16]  P. C. Struik,et al.  Cisgenesis Does Not Solve the Late Blight Problem of Organic Potato Production: Alternative Breeding Strategies , 2008, Potato Research.

[17]  Gert Jan Hofstede,et al.  Analysing potato late blight control as a social-ecological system using fuzzy cognitive mapping , 2016, Agronomy for Sustainable Development.

[18]  Understanding obstacles and opportunities for successful market introduction of crop varieties with resistance against major diseases , 2018, Organic Agriculture.

[19]  B. Schöber,et al.  Recent and future developments in potato fungal pathology , 1992, Netherlands Journal of Plant Pathology.

[20]  A. J. Haverkort,et al.  Durable Late Blight Resistance in Potato Through Dynamic Varieties Obtained by Cisgenesis: Scientific and Societal Advances in the DuRPh Project , 2016, Potato Research.

[21]  W. van der Werf,et al.  Achieving Durable Resistance Against Plant Diseases: Scenario Analyses with a National-Scale Spatially Explicit Model for a Wind-Dispersed Plant Pathogen. , 2017, Phytopathology.

[22]  G. Gilbert Evolutionary ecology of plant diseases in natural ecosystems. , 2002, Annual review of phytopathology.

[23]  C. Gilligan,et al.  Measures of durability of resistance. , 2003, Phytopathology.

[24]  J. Gareth Polhill,et al.  The ODD protocol: A review and first update , 2010, Ecological Modelling.

[25]  Wopke van der Werf,et al.  Invasion of Phytophthora infestans at the landscape level: how do spatial scale and weather modulate the consequences of spatial heterogeneity in host resistance? , 2010, Phytopathology.

[26]  A. J. Haverkort,et al.  Societal Costs of Late Blight in Potato and Prospects of Durable Resistance Through Cisgenic Modification , 2008, Potato Research.

[27]  M. Oijen Evaluation of breeding strategies for resistance and tolerance to late blight in potato by means of simulation , 2005, Netherlands Journal of Plant Pathology.

[28]  C. Mundt Durable resistance: a key to sustainable management of pathogens and pests. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[29]  Birgit Müller,et al.  A standard protocol for describing individual-based and agent-based models , 2006 .

[30]  B. J. Nielsen,et al.  Epidemiology and Integrated Control of Potato Late Blight in Europe , 2011, Potato Research.

[31]  Li An,et al.  Modeling human decisions in coupled human and natural systems: Review of agent-based models , 2012 .

[32]  Karen A. Garrett,et al.  Why dispersal should be maximized at intermediate scales of heterogeneity , 2012, Theoretical Ecology.

[33]  Arend Ligtenberg,et al.  Which Sensitivity Analysis Method Should I Use for My Agent-Based Model? , 2016, J. Artif. Soc. Soc. Simul..

[34]  A. Haverkort,et al.  A model for potato growth and yield under tropical highland conditions , 1987 .

[35]  Pink,et al.  Deployment of disease resistance genes by plant transformation - a 'mix and match' approach. , 1999, Trends in plant science.

[36]  W. Rossing,et al.  Parameterization and evaluation of a spatiotemporal model of the potato late blight pathosystem. , 2009, Phytopathology.

[37]  S. Solberg,et al.  Assessment of the Socio-Economic Impact of Late Blight and State-of-the-Art Management in European Organic Potato Production Systems , 2004 .

[38]  F. Govers,et al.  Development of potato late blight epidemics: disease foci, disease gradients, and infection sources. , 1998, Phytopathology.

[39]  Fyodor A Kondrashov,et al.  Measurements of spontaneous rates of mutations in the recent past and the near future , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[40]  L. Hossard,et al.  Linking cropping system mosaics to disease resistance durability , 2015 .