Differential impact of landscape‐scale strategies for crop cultivar deployment on disease dynamics, resistance durability and long‐term evolutionary control

A multitude of resistance deployment strategies have been proposed to tackle the evolutionary potential of pathogens to overcome plant resistance. In particular, many landscape‐based strategies rely on the deployment of resistant and susceptible cultivars in an agricultural landscape as a mosaic. However, the design of such strategies is not easy as strategies targeting epidemiological or evolutionary outcomes may not be the same. Using a stochastic spatially explicit model, we studied the impact of landscape organization (as defined by the proportion of fields cultivated with a resistant cultivar and their spatial aggregation) and key pathogen life‐history traits on three measures of disease control. Our results show that short‐term epidemiological dynamics are optimized when landscapes are planted with a high proportion of the resistant cultivar in low aggregation. Importantly, the exact opposite situation is optimal for resistance durability. Finally, well‐mixed landscapes (balanced proportions with low aggregation) are optimal for long‐term evolutionary equilibrium (defined here as the level of long‐term pathogen adaptation). This work offers a perspective on the potential for contrasting effects of landscape organization on different goals of disease management and highlights the role of pathogen life history.

[1]  W. 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 .

[2]  J. Burdon,et al.  Addressing the Challenges of Pathogen Evolution on the World's Arable Crops. , 2016, Phytopathology.

[3]  L. Mailleret,et al.  Epidemiological and evolutionary management of plant resistance: optimizing the deployment of cultivar mixtures in time and space in agricultural landscapes , 2015, Evolutionary applications.

[4]  James K. M. Brown.  Durable resistance of crops to disease: a Darwinian perspective. , 2015, Annual review of phytopathology.

[5]  J. Burdon,et al.  Playing on a pathogen's weakness: using evolution to guide sustainable plant disease control strategies. , 2015, Annual review of phytopathology.

[6]  T. Marcel,et al.  Quantitative resistance to biotrophic filamentous plant pathogens: concepts, misconceptions, and mechanisms. , 2015, Annual review of phytopathology.

[7]  J. Burdon,et al.  Crop pathogen emergence and evolution in agro-ecological landscapes , 2015, Evolutionary applications.

[8]  L. Chaumont,et al.  Sustainable deployment of QTLs conferring quantitative resistance to crops: first lessons from a stochastic model. , 2014, The New phytologist.

[9]  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.

[10]  Hervé Monod,et al.  Pathogen population dynamics in agricultural landscapes: the Ddal modelling framework. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[11]  B. Le Cam,et al.  When virulence originates from non-agricultural hosts: new insights into plant breeding. , 2014, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[12]  J. Burdon,et al.  Achieving sustainable plant disease management through evolutionary principles. , 2014, Trends in plant science.

[13]  Hervé Monod,et al.  Can epidemic control be achieved by altering landscape connectivity in agricultural systems , 2014 .

[14]  Otso Ovaskainen,et al.  Ecological and evolutionary effects of fragmentation on infectious disease dynamics , 2014, Science.

[15]  Xianming Chen,et al.  Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. , 2014, Molecular plant pathology.

[16]  G. Rebetzke,et al.  Guiding deployment of resistance in cereals using evolutionary principles , 2014, Evolutionary applications.

[17]  Peter H. Thrall,et al.  Evolution of Pathogen Specialisation in a Host Metapopulation: Joint Effects of Host and Pathogen Dispersal , 2014, PLoS Comput. Biol..

[18]  C. Gilligan,et al.  Quantitative resistance can lead to evolutionary changes in traits not targeted by the resistance QTLs , 2014, Evolutionary applications.

[19]  A. Tack,et al.  Ecological and evolutionary implications of spatial heterogeneity during the off-season for a wild plant pathogen , 2013, The New phytologist.

[20]  Anna‐Liisa Laine,et al.  Epidemiological and evolutionary consequences of life‐history trade‐offs in pathogens , 2013 .

[21]  L. Chaumont,et al.  Timing of Pathogen Adaptation to a Multicomponent Treatment , 2013, PloS one.

[22]  H. Monod,et al.  Dynamics of Adaptation in Spatially Heterogeneous Metapopulations , 2013, PloS one.

[23]  K. Kiêu,et al.  A completely random T-tessellation model and Gibbsian extensions , 2013, 1302.1809.

[24]  A. Palloix,et al.  Virus adaptation to quantitative plant resistance: erosion or breakdown? , 2012, Journal of evolutionary biology.

[25]  I. Sache,et al.  Components of quantitative resistance to leaf rust in wheat cultivars: diversity, variability and specificity , 2012 .

[26]  G. Azzimonti.  Diversification de la résistance quantitative à la rouille brune du blé, à partir de la caractérisation des composantes de la résistance , 2012 .

[27]  F. C. van den Bosch,et al.  The evolution of plant pathogens in response to host resistance: factors affecting the gain from deployment of qualitative and quantitative resistance. , 2012, Journal of theoretical biology.

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

[29]  A. Bennett,et al.  Meeting the demand for crop production: the challenge of yield decline in crops grown in short rotations , 2012, Biological reviews of the Cambridge Philosophical Society.

[30]  Mevin B Hooten,et al.  Forest species diversity reduces disease risk in a generalist plant pathogen invasion. , 2011, Ecology letters.

[31]  A. Arneth,et al.  Representing human behaviour and decisional processes in land system models as an integral component of the earth system , 2011 .

[32]  J. Oakeshott,et al.  Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems , 2011, Evolutionary applications.

[33]  C. Lannou,et al.  Specific resistance to leaf rust expressed at the seedling stage in cultivars grown in France from 1983 to 2007 , 2011, Euphytica.

[34]  S. Gandon,et al.  Evolution in Heterogeneous Environments: Between Soft and Hard Selection , 2011, The American Naturalist.

[35]  J. Burdon,et al.  Spatial variation in disease resistance: from molecules to metapopulations , 2011, The Journal of ecology.

[36]  R. Arditi,et al.  Spatially mixed crops to control the stratified dispersal of airborne fungal diseases , 2010 .

[37]  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.

[38]  S. Gandon,et al.  Evolution of specialization in a spatially continuous environment , 2010, Journal of evolutionary biology.

[39]  G. Marion,et al.  Species' Range: Adaptation in Space and Time , 2009, The American Naturalist.

[40]  Ulf Dieckmann,et al.  Live Where You Thrive: Joint Evolution of Habitat Choice and Local Adaptation Facilitates Specialization and Promotes Diversity , 2009, The American Naturalist.

[41]  S Soubeyrand,et al.  Spatiotemporal Structure of Host‐Pathogen Interactions in a Metapopulation , 2009, The American Naturalist.

[42]  Hervé Monod,et al.  Computation of the integrated flow of particles between polygons , 2009, Environ. Model. Softw..

[43]  C. Lannou,et al.  Aggressiveness components and adaptation to a host cultivar in wheat leaf rust. , 2009, Phytopathology.

[44]  C. Lannou,et al.  Aggressiveness and its role in the adaptation of plant pathogens , 2009 .

[45]  J. Burdon,et al.  Coevolution of Plants and Their Pathogens in Natural Habitats , 2009, Science.

[46]  G. McDonald,et al.  Effects of crop rotation, residue retention and sowing time on the incidence and survival of ascochyta blight and its effect on grain yield of field peas (Pisum sativum L.). , 2009 .

[47]  Christopher A Gilligan,et al.  Epidemiological models for invasion and persistence of pathogens. , 2008, Annual review of phytopathology.

[48]  R. Park.  Breeding cereals for rust resistance in Australia , 2008 .

[49]  Bruno Sudret,et al.  Global sensitivity analysis using polynomial chaos expansions , 2008, Reliab. Eng. Syst. Saf..

[50]  Leslie A Real,et al.  Spatial dynamics and genetics of infectious diseases on heterogeneous landscapes , 2007, Journal of The Royal Society Interface.

[51]  Manuel Plantegenest,et al.  Landscape epidemiology of plant diseases , 2007, Journal of The Royal Society Interface.

[52]  Ross K. Meentemeyer,et al.  Effects of landscape heterogeneity on the emerging forest disease sudden oak death , 2007 .

[53]  J. Burdon,et al.  Epidemiological patterns at multiple spatial scales: an 11‐year study of a Triphragmium ulmariae– Filipendula ulmaria metapopulation , 2003 .

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

[55]  J. Burdon,et al.  Evolution of Virulence in a Plant Host-Pathogen Metapopulation , 2003, Science.

[56]  J. Parlevliet.  Durability of resistance against fungal, bacterial and viral pathogens; present situation , 2002, Euphytica.

[57]  Sylvain Gandon,et al.  Imperfect vaccines and the evolution of pathogen virulence , 2001, Nature.

[58]  Lenore Fahrig,et al.  Landscape structure influences continental distribution of hantavirus in deer mice , 2001, Landscape Ecology.

[59]  Youyong Zhu,et al.  Genetic diversity and disease control in rice , 2000, Nature.

[60]  Chancellor,et al.  Modelling the spatio‐temporal deployment of resistant varieties to reduce the incidence of rice tungro disease in a dynamic cropping system , 1999 .

[61]  J. Burdon,et al.  Spatial and Temporal Patterns in Coevolving Plant and Pathogen Associations , 1999, The American Naturalist.

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

[63]  Christian Lannou,et al.  Variation and selection of quantitative traits in plant pathogens. , 2012, Annual review of phytopathology.

[64]  ichard,et al.  THE EFFECT OF FOREST FRAGMENTATION ON LYME DISEASE RISK , 2011 .

[65]  S. Powers,et al.  Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. , 2010, The New phytologist.

[66]  D. Stuthman,et al.  Breeding Crops for Durable Resistance to Disease , 2007 .

[67]  S. Pietravalle,et al.  Durability of Resistance and Cost of Virulence , 2005, European Journal of Plant Pathology.

[68]  T. Doré,et al.  Agronomic approach: cropping systems and plant diseases. , 2003, Comptes rendus biologies.

[69]  C. Mundt.  Use of multiline cultivars and cultivar mixtures for disease management. , 2002, Annual review of phytopathology.

[70]  H. Leung,et al.  Pathogen fitness penalty as a predictor of durability of disease resistance genes. , 2001, Annual review of phytopathology.

[71]  P. E. Waggoner,et al.  Defoliation, disease, and growth , 1987 .

[72]  C. Mundt,et al.  Computerized simulation of crown rust epidemics in mixtures of immune and susceptible oat plants with different genotype unit areas and spatial distributions of initial disease , 1986 .

[73]  R. Johnson.  A critical analysis of durable resistance , 1984 .

[74]  Hh Flor,et al.  Host-parasite interaction in flax rust–its genetics and other implications , 1955 .