Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemma

Adult plant resistance (APR) is an incomplete and delayed protection of plants against pathogens. At first glance, such resistance should be less efficient than classical major-effect resistance genes, which confer complete resistance from seedling stage, to reduce epidemics. However, by allowing some ‘leaky’ levels of disease, APR genes are predicted to be more durable than major genes because they exert a weaker selection pressure on pathogens towards adaptation to resistance. However, the impact of partial efficiency and delayed mode of action of APR on the evolutionary and epidemiological outcomes of resistance deployment has never been tested. Using the demogenetic, spatially explicit, temporal, stochastic model landsepi, this study is a first attempt to investigate how resistance efficiency, age at the time of resistance activation and target pathogenicity trait jointly impact resistance durability and disease control at the landscape scale. Our numerical experiments explore the deployment of APR in a simulated agricultural landscape, alone or together with a major resistance gene. As a case study, the mathematical model has been parameterised for rust fungi (genus Puccinia) of cereal crops, for which extensive data are available. Our simulations confirm that weak efficiency and delayed activation of APR genes reduce the selection pressure applied on pathogens and their propensity to overcome resistance, but do not confer effective protection. On the other hand, stronger APR genes (which increase selection pressure on the pathogen) may be quickly overcome but have the potential to provide some disease protection in the short-term. This is attributed to strong competition between different pathogen genotypes and the presence of fitness costs of adaptation, especially when APR genes are deployed together with a major resistance gene via crop mixtures or rotations.

[1]  T. Poisot Plant resistance to pathogens: just you wait? , 2023, Peer Community in Evolutionary Biology.

[2]  F. Grognard,et al.  Improving sustainable crop protection using population genetics concepts , 2022, Molecular ecology.

[3]  C. Hackett,et al.  Phloem connectivity and transport are not involved in mature plant resistance (MPR) to Potato Virus Y in different potato cultivars, and MPR does not protect tubers from recombinant strains of the virus. , 2022, Journal of plant physiology.

[4]  F. Grognard,et al.  Host mixtures for plant disease control: Benefits from pathogen selection and immune priming , 2022, Evolutionary applications.

[5]  J. Papaïx,et al.  Models of Plant Resistance Deployment. , 2021, Annual review of phytopathology.

[6]  F. Grognard,et al.  Taking advantage of pathogen diversity and immune priming to minimize disease prevalence in host mixtures: a model. , 2020, Phytopathology.

[7]  M. Renton,et al.  Rotating and stacking genes can improve crop resistance durability while potentially selecting highly virulent pathogen strains , 2020, Scientific Reports.

[8]  F. Hamelin,et al.  Assessing the effects of quantitative host resistance on the life-history traits of sporulating parasites with growing lesions , 2019, Proceedings of the Royal Society B.

[9]  C. Gilligan,et al.  When does spatial diversification usefully maximise the durability of crop disease resistance? , 2019, bioRxiv.

[10]  S. German-Retana,et al.  Role of the Genetic Background in Resistance to Plant Viruses , 2018, International journal of molecular sciences.

[11]  J. Burdon,et al.  Mosaics, mixtures, rotations or pyramiding: What is the optimal strategy to deploy major gene resistance? , 2018, Evolutionary applications.

[12]  C. Mundt Pyramiding for Resistance Durability: Theory and Practice. , 2018, Phytopathology.

[13]  Jean-François Rey,et al.  Assessing the durability and efficiency of landscape-based strategies to deploy plant resistance to pathogens , 2018, bioRxiv.

[14]  J. Burdon,et al.  Differential impact of landscape‐scale strategies for crop cultivar deployment on disease dynamics, resistance durability and long‐term evolutionary control , 2017, Evolutionary applications.

[15]  S. Fournet,et al.  Quantitative Resistance to Plant Pathogens in Pyramiding Strategies for Durable Crop Protection , 2017, Front. Plant Sci..

[16]  F. Fabre,et al.  Mosaics often outperform pyramids: insights from a model comparing strategies for the deployment of plant resistance genes against viruses in agricultural landscapes. , 2017, The New phytologist.

[17]  F. C. van den Bosch,et al.  Extending the durability of cultivar resistance by limiting epidemic growth rates , 2017, Proceedings of the Royal Society B: Biological Sciences.

[18]  R. Oliva,et al.  Immunity and starvation: new opportunities to elevate disease resistance in crops. , 2017, Current opinion in plant biology.

[19]  B. Keller,et al.  Molecular genetics and evolution of disease resistance in cereals. , 2016, The New phytologist.

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

[21]  J. Patrick,et al.  A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat , 2015, Nature Genetics.

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

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

[24]  S. Bonhoeffer,et al.  Developing smarter host mixtures to control plant disease , 2015 .

[25]  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.

[26]  M. Hovmøller,et al.  New Races of Puccinia striiformis Found in Europe Reveal Race Specificity of Long-Term Effective Adult Plant Resistance in Wheat. , 2014, Phytopathology.

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

[28]  R. Kormelink,et al.  Dominant resistance against plant viruses , 2014, Front. Plant Sci..

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

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

[31]  F. C. van den Bosch,et al.  The Emergence of Resistance to Fungicides , 2014, PloS one.

[32]  J. Burdon,et al.  What have we learned from studies of wild plant-pathogen associations?—the dynamic interplay of time, space and life-history , 2014, European Journal of Plant Pathology.

[33]  Yan Guo,et al.  Mapping of QTL lengthening the latent period of Puccinia striiformis in winter wheat at the tillering growth stage , 2013, European Journal of Plant Pathology.

[34]  Maqsood Qamar,et al.  Determination of Rust Resistance Gene Complex Lr34/Yr18 in Spring Wheat and its Effect on Components of Partial Resistance , 2012 .

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

[36]  M. Heil,et al.  Unifying concepts and mechanisms in the specificity of plant-enemy interactions. , 2012, Trends in plant science.

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

[38]  A. Sasaki,et al.  How does the resistance threshold in spatially explicit epidemic dynamics depend on the basic reproductive ratio and spatial correlation of crop genotypes? , 2011, Journal of theoretical biology.

[39]  G. Ash Wheat Rusts: An Atlas of Resistance Genes. , 1996, Australasian Plant Pathology.

[40]  Alain Palloix,et al.  L'adaptation des virus de plantes aux résistances variétales , 2010 .

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

[42]  J. Dubcovsky,et al.  A Kinase-START Gene Confers Temperature-Dependent Resistance to Wheat Stripe Rust , 2009, Science.

[43]  B. Keller,et al.  A Putative ABC Transporter Confers Durable Resistance to Multiple Fungal Pathogens in Wheat , 2009, Science.

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

[45]  Christopher A Gilligan,et al.  Sustainable agriculture and plant diseases: an epidemiological perspective , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  E. Galiana,et al.  Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom. , 2007, The New phytologist.

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

[48]  L. Broers,et al.  Quantitative resistance and its components in 16 barley cultivars to yellow rust, Puccinia striiformis f. sp. hordei , 2007, Euphytica.

[49]  C. Mundt,et al.  Pyramiding and dissecting disease resistance QTL to barley stripe rust , 2006, Theoretical and Applied Genetics.

[50]  R. Ostfeld,et al.  Effects of species diversity on disease risk. , 2006, Ecology letters.

[51]  L. Boyd Can Robigus defeat an old enemy? – Yellow rust of wheat , 2005, The Journal of Agricultural Science.

[52]  Xianming Chen,et al.  Epidemiology and control of stripe rust [Puccinia striiformis f. sp. tritici] on wheat , 2005 .

[53]  C. Lannou,et al.  Effect of host genotype on leaf rust (Puccinia triticina) lesion development and urediniospore production in wheat seedlings , 2005 .

[54]  J. Tewari,et al.  Assessment of Two Different Sources of Durable Resistance and Susceptible Cultivar of Wheat to Stripe Rust (Puccinia striiformis f. sp. tritici) , 2005 .

[55]  A. Calonnec,et al.  Effects of induced resistance on infection efficiency and sporulation of Puccinia striiformis on seedlings in varietal mixtures and on field epidemics in pure stands , 1996, European Journal of Plant Pathology.

[56]  M. Oijen Selection and use of a mathematical model to evaluate components of resistance to Phytophthora infestans in potato , 1992, Netherlands Journal of Plant Pathology.

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

[58]  B. Wiggins,et al.  Temporal expression of PR-1 and enhanced mature plant resistance to virus infection is controlled by a single dominant gene in a new Nicotiana hybrid. , 2004, Molecular plant-microbe interactions : MPMI.

[59]  A. Palloix,et al.  Durable virus resistance in plants through conventional approaches: a challenge. , 2004, Virus research.

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

[61]  L. Broers Components of quantitative resistance to yellow rust in ten spring bread wheat cultivars and their relations with field assessments , 1997, Euphytica.

[62]  D. Singh,et al.  Relative importance of components affecting the leaf rust progress curve in wheat , 1982, Theoretical and Applied Genetics.

[63]  L. Broers,et al.  Field assessment of quantitative resistance to yellow rust in ten spring bread wheat cultivars , 2004, Euphytica.

[64]  C. Denissen Components of adult plant resistance to leaf rust in wheat , 2004, Euphytica.

[65]  C. Mundt,et al.  Methods for estimating epidemiological effects of quantitative resistance to plant diseases , 2004, Theoretical and Applied Genetics.

[66]  B. McDonald,et al.  An analysis of the durability of resistance to plant viruses. , 2003, Phytopathology.

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

[68]  B. McDonald,et al.  Pathogen population genetics, evolutionary potential, and durable resistance. , 2002, Annual review of phytopathology.

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

[70]  John F. Murphy,et al.  Age‐related Resistance in Bell Pepper to Cucumber mosaic virus , 2001 .

[71]  K. Sayre,et al.  Estimating the Economic Impact of Breeding Nonspecific Resistance to Leaf Rust in Modern Bread Wheats. , 1998, Plant disease.

[72]  R. Singh,et al.  Expression of adult resistance to stripe rust at different growth stages of wheat , 1996 .

[73]  J. S. Lehman Genetic Variation in Latent Period Among Isolates of Puccinia recondita f. sp. tritici on Partially Resistant Wheat Cultivars , 1996 .

[74]  I. Sache,et al.  Classification of airborne plant pathogens based on sporulation and infection characteristics , 1995 .

[75]  R. Park,et al.  Wheat Rusts: An Atlas of Resistance Genes , 1995 .

[76]  L. Fahrig,et al.  Connectivity is a vital element of landscape structure , 1993 .

[77]  M. Cromey Adult plant resistance to stripe rust (Puccinia striiformis) in some New Zealand wheat cultivars , 1992 .

[78]  R. Park,et al.  Expression of adult plant resistance and its effect on the development of Puccinia striiformis f.sp. tritici in some Australian wheat cultivars , 1989 .

[79]  N. Huntly,et al.  Diseases and plant population biology , 1988 .

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

[81]  J. R. Tomerlin,et al.  Temperature and Host Effects on Latent and Infectious Periods and on Urediniospore Production ofPuccinia reconditaf. sp.tritici , 1983 .

[82]  R. Johnson Genetic Background of Durable Resistance , 1983 .

[83]  J. Parlevliet Components of Resistance that Reduce the Rate of Epidemic Development , 1979 .

[84]  G. Green,et al.  Assessment of receptivity and urediospore production as components of wheat stem rust resistance , 1978 .

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