Section: Evolutionary Biology
Topic: Evolution, Plant biology

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

10.24072/pcjournal.271 - Peer Community Journal, Volume 3 (2023), article no. e43.

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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.

Published online:
DOI: 10.24072/pcjournal.271
Type: Research article
Keywords: adaptation, adult plant resistance, disease control, immunity, mature plant resistance, ontogenic, puccinia, resistance, resistance durability, rust, simulation modelling.
Rimbaud, Loup 1; Papaïx, Julien 2; Rey, Jean-François 2; Moury, Benoît 1; Barrett, Luke G. 3; Thrall, Peter H. 4

1 INRAE Pathologie Végétale, 84143 Montfavet, France
2 INRAE BioSP, 84914 Avignon, France
3 CSIRO Agriculture and Food, Canberra 2601 ACT, Australia
4 CSIRO National Collections & Marine Infrastructure, Canberra 2601 ACT, Australia
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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     title = {Durable resistance or efficient disease control? {Adult} {Plant} {Resistance} {(APR)} at the heart of the dilemma},
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Rimbaud, Loup; Papaïx, Julien; Rey, Jean-François; Moury, Benoît; Barrett, Luke G.; Thrall, Peter H. Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemma. Peer Community Journal, Volume 3 (2023), article  no. e43. doi : 10.24072/pcjournal.271. https://peercommunityjournal.org/articles/10.24072/pcjournal.271/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100628

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Azzimonti, G.; Lannou, C.; Sache, I.; Goyeau, H. Components of quantitative resistance to leaf rust in wheat cultivars: diversity, variability and specificity, Plant Pathology, Volume 62 (2013) no. 5, pp. 970-981 | DOI

[2] Barrett, L. G.; Heil, M. Unifying concepts and mechanisms in the specificity of plant–enemy interactions, Trends in Plant Science, Volume 17 (2012) no. 5, pp. 282-292 | DOI

[3] Boyd, L. A. Can Robigus defeat an old enemy? – Yellow rust of wheat, The Journal of Agricultural Science, Volume 143 (2005) no. 4, pp. 233-243 | DOI

[4] Broers, L. Euphytica, 96 (1997) no. 2, pp. 215-223 | DOI

[5] Broers, L. H. M.; Cuesta Subias, X.; López Atilano, R. M. Field assessment of quantitative resistance to yellow rust in ten spring bread wheat cultivars, Euphytica, Volume 90 (1996) no. 1, pp. 9-16 | DOI

[6] Burdon, J. Diseases and Plant Population Biology, Cambridge University Press, Cambridge, 1987, 56 pages

[7] Burdon, J. J.; Barrett, L. G.; Rebetzke, G.; Thrall, P. H. Guiding deployment of resistance in cereals using evolutionary principles, Evolutionary Applications, Volume 7 (2014) no. 6, pp. 609-624 | DOI

[8] Burdon, J. J.; Thrall, P. H. What have we learned from studies of wild plant-pathogen associations?—the dynamic interplay of time, space and life-history, European Journal of Plant Pathology, Volume 138 (2013) no. 3, pp. 417-429 | DOI

[9] Burdon, J. J.; Zhan, J.; Barrett, L. G.; Papaïx, J.; Thrall, P. H. Addressing the Challenges of Pathogen Evolution on the World’s Arable Crops, Phytopathology®, Volume 106 (2016) no. 10, pp. 1117-1127 | DOI

[10] Calonnec, A.; Goyeau, H.; de Vallavieille-Pope, C. Effects of induced resistance on infection efficiency and sporulation of Puccinia striiformis on seedlings in varietal mixtures and on field epidemics in pure stands, European Journal of Plant Pathology, Volume 102 (1996) no. 8, pp. 733-741 | DOI

[11] Carolan, K.; Helps, J.; van den Berg, F.; Bain, R.; Paveley, N.; van den Bosch, F. Extending the durability of cultivar resistance by limiting epidemic growth rates, Proceedings of the Royal Society B: Biological Sciences, Volume 284 (2017) no. 1863 | DOI

[12] Chen, W.; Wellings, C.; Chen, X.; Kang, Z.; Liu, T. Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici , Molecular Plant Pathology, Volume 15 (2014) no. 5, pp. 433-446 | DOI

[13] Chen, X. Epidemiology and control of stripe rust [Puccinia striiformis f. sp.tritici] on wheat, Canadian Journal of Plant Pathology, Volume 27 (2005) no. 3, pp. 314-337 | DOI

[14] Clin, P.; Grognard, F.; Andrivon, D.; Mailleret, L.; Hamelin, F. M. Host mixtures for plant disease control: Benefits from pathogen selection and immune priming, Evolutionary Applications, Volume 15 (2022) no. 6, pp. 967-975 | DOI

[15] Clin, P.; Grognard, F.; Mailleret, L.; Val, F.; Andrivon, D.; Hamelin, F. M. Taking Advantage of Pathogen Diversity and Immune Priming to Minimize Disease Prevalence in Host Mixtures: A Model, Phytopathology, Volume 111 (2021) no. 7, pp. 1219-1227 | DOI

[16] Cole, A. B.; Király, L.; Lane, L. C.; Wiggins, B. E.; Ross, K.; Schoelz, J. E. 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, Molecular Plant-Microbe Interactions, Volume 17 (2004) no. 9, pp. 976-985 | DOI

[17] Crété, R.; Pires, R. N.; Barbetti, M. J.; Renton, M. Rotating and stacking genes can improve crop resistance durability while potentially selecting highly virulent pathogen strains, Scientific Reports, Volume 10 (2020) no. 1 | DOI

[18] Cromey, M. G. Adult plant resistance to stripe rust (Puccinia striiformis) in some New Zealand wheat cultivars, New Zealand Journal of Crop and Horticultural Science, Volume 20 (1992) no. 4, pp. 413-419 | DOI

[19] de Ronde, D.; Butterbach, P.; Kormelink, R. Dominant resistance against plant viruses, Frontiers in Plant Science, Volume 5 (2014) | DOI

[20] Denissen, C. J. M. Components of adult plant resistance to leaf rust in wheat, Euphytica, Volume 70 (1993) no. 1-2, pp. 131-140 | DOI

[21] Develey‐Rivière, M.; Galiana, E. Resistance to pathogens and host developmental stage: a multifaceted relationship within the plant kingdom, New Phytologist, Volume 175 (2007) no. 3, pp. 405-416 | DOI

[22] Djidjou‐Demasse, R.; Moury, B.; Fabre, F. Mosaics often outperform pyramids: insights from a model comparing strategies for the deployment of plant resistance genes against viruses in agricultural landscapes, New Phytologist, Volume 216 (2017) no. 1, pp. 239-253 | DOI

[23] Elahinia, S.; Tewari, J. Assessment of two different sources of durable resistance and susceptible cultivar of wheat to stripe rust (Puccinia striiformis f. sp. tritici), Caspian Journal of Environmental Sciences, Volume 3 (2005), pp. 117-122 (http://cjes.guilan.ac.ir/article_948_5e0230f27bfd99b837bd4d79b5fd8591.pdf)

[24] Flor, H. Host-parasite interaction in flax rust - Its genetics and other implications, Phytopathology, Volume 45 (1955), pp. 680-685 (https://ethz.ch/content/dam/ethz/special-interest/usys/ibz/theoreticalbiology/education/learningmaterials/701-0263-01L/Flor1955_Phytopathology_Host_parasite_interaction_genetics.pdf)

[25] Fu, D.; Uauy, C.; Distelfeld, A.; Blechl, A.; Epstein, L.; Chen, X.; Sela, H.; Fahima, T.; Dubcovsky, J. A Kinase-START Gene Confers Temperature-Dependent Resistance to Wheat Stripe Rust, Science, Volume 323 (2009) no. 5919, pp. 1357-1360 | DOI

[26] Gallois, J.-L.; Moury, B.; German-Retana, S. Role of the Genetic Background in Resistance to Plant Viruses, International Journal of Molecular Sciences, Volume 19 (2018) no. 10 | DOI

[27] García-Arenal, F.; McDonald, B. A. An Analysis of the Durability of Resistance to Plant Viruses, Phytopathology®, Volume 93 (2003) no. 8, pp. 941-952 | DOI

[28] Garcia-Ruiz, H.; Murphy, J. F. Age-related Resistance in Bell Pepper to Cucumber mosaic virus, Annals of Applied Biology, Volume 139 (2001) no. 3, pp. 307-317 | DOI

[29] Gilligan, C. A. Sustainable agriculture and plant diseases: an epidemiological perspective, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 363 (2008) no. 1492, pp. 741-759 | DOI

[30] Hobbelen, P. H. F.; Paveley, N. D.; van den Bosch, F. The Emergence of Resistance to Fungicides, PLoS ONE, Volume 9 (2014) no. 3 | DOI

[31] Johnson, R. Genetic Background of Durable Resistance, Durable Resistance in Crops, Springer New York, Boston, MA, 1983, pp. 5-26 | DOI

[32] Johnson, R. A Critical Analysis of Durable Resistance, Annual Review of Phytopathology, Volume 22 (1984) no. 1, pp. 309-330 | DOI

[33] Keesing, F.; Holt, R. D.; Ostfeld, R. S. Effects of species diversity on disease risk, Ecology Letters, Volume 9 (2006) no. 4, pp. 485-498 | DOI

[34] Krattinger, S. G.; Keller, B. Molecular genetics and evolution of disease resistance in cereals, New Phytologist, Volume 212 (2016) no. 2, pp. 320-332 | DOI

[35] Krattinger, S. G.; Lagudah, E. S.; Spielmeyer, W.; Singh, R. P.; Huerta-Espino, J.; McFadden, H.; Bossolini, E.; Selter, L. L.; Keller, B. A Putative ABC Transporter Confers Durable Resistance to Multiple Fungal Pathogens in Wheat, Science, Volume 323 (2009) no. 5919, pp. 1360-1363 | DOI

[36] Kulkarni, R. N.; Chopra, V. L.; Singh, D. Relative importance of components affecting the leaf rust progress curve in wheat, Theoretical and Applied Genetics, Volume 62 (1982) no. 3, pp. 205-207 | DOI

[37] Kumar, P.; Cowan, G. H.; Squires, J. N.; Hackett, C. A.; Tobin, A. K.; Torrance, L.; Roberts, A. G. 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, Journal of Plant Physiology, Volume 275 (2022) | DOI

[38] Lannou, C. Variation and Selection of Quantitative Traits in Plant Pathogens, Annual Review of Phytopathology, Volume 50 (2012) no. 1, pp. 319-338 | DOI

[39] Leclerc, M.; Clément, J. A. J.; Andrivon, D.; Hamelin, F. M. Assessing the effects of quantitative host resistance on the life-history traits of sporulating parasites with growing lesions, Proceedings of the Royal Society B: Biological Sciences, Volume 286 (2019) no. 1912 | DOI

[40] Lecoq, H.; Moury, B.; Desbiez, C.; Palloix, A.; Pitrat, M. Durable virus resistance in plants through conventional approaches: a challenge, Virus Research, Volume 100 (2004) no. 1, pp. 31-39 | DOI

[41] Lehman, J. Genetic Variation in Latent Period Among Isolates of Puccinia recondita f. sp. tritici on Partially Resistant Wheat Cultivars, Phytopathology, Volume 86 (1996) no. 6 | DOI

[42] Leonard, K. J.; Mundt, C. C. Methods for estimating epidemiological effects of quantitative resistance to plant diseases, Theoretical and Applied Genetics, Volume 67 (1984) no. 2-3, pp. 219-230 | DOI

[43] Ma, H. Expression of Adult Resistance to Stripe Rust at Different Growth Stages of Wheat, Plant Disease, Volume 80 (1996) no. 4 | DOI

[44] McDonald, B. A.; Linde, C. Pathogen population genetics, evolutionary potential, and durable resistance, Annual Review of Phytopathology, Volume 40 (2002) no. 1, pp. 349-379 | DOI

[45] McIntosh, R.; Wellings, C.; Park, R. Wheat Rusts, CSIRO Publishing, 1995 | DOI

[46] Mikaberidze, A.; McDonald, B. A.; Bonhoeffer, S. Developing smarter host mixtures to control plant disease, Plant Pathology, Volume 64 (2014) no. 4, pp. 996-1004 | DOI

[47] Moore, J. W.; Herrera-Foessel, S.; Lan, C.; Schnippenkoetter, W.; Ayliffe, M.; Huerta-Espino, J.; Lillemo, M.; Viccars, L.; Milne, R.; Periyannan, S.; Kong, X.; Spielmeyer, W.; Talbot, M.; Bariana, H.; Patrick, J. W.; Dodds, P.; Singh, R.; Lagudah, E. A recently evolved hexose transporter variant confers resistance to multiple pathogens in wheat, Nature Genetics, Volume 47 (2015) no. 12, pp. 1494-1498 | DOI

[48] Mortensen, K.; Green, G. J. Assessment of receptivity and urediospore production as components of wheat stem rust resistance, Canadian Journal of Botany, Volume 56 (1978) no. 16, pp. 1827-1839 | DOI

[49] Moury, B.; Fabre, F.; Montarry, J.; Janzac, B.; Ayme, V.; Palloix, A. L’adaptation des virus de plantes aux résistances variétales, Virologie, Volume 14 (2010), pp. 227-239 (https://hal.inrae.fr/hal-02669234)

[50] Mundt, C. C. Use of multiline cultivars and cultivar mixtures for disease management, Annual Review of Phytopathology, Volume 40 (2002) no. 1, pp. 381-410 | DOI

[51] Mundt, C. C. Pyramiding for Resistance Durability: Theory and Practice, Phytopathology, Volume 108 (2018) no. 7, pp. 792-802 | DOI

[52] Niks, R. E.; Qi, X.; Marcel, T. C. Quantitative Resistance to Biotrophic Filamentous Plant Pathogens: Concepts, Misconceptions, and Mechanisms, Annual Review of Phytopathology, Volume 53 (2015) no. 1, pp. 445-470 | DOI

[53] Oliva, R.; Quibod, I. L. Immunity and starvation: new opportunities to elevate disease resistance in crops, Current Opinion in Plant Biology, Volume 38 (2017), pp. 84-91 | DOI

[54] Papaïx, J.; Adamczyk-Chauvat, K.; Bouvier, A.; Kiêu, K.; Touzeau, S.; Lannou, C.; Monod, H. Pathogen population dynamics in agricultural landscapes: The Ddal modelling framework, Infection, Genetics and Evolution, Volume 27 (2014), pp. 509-520 | DOI

[55] Papaïx, J.; Rimbaud, L.; Burdon, J. J.; Zhan, J.; Thrall, P. H. Differential impact of landscape-scale strategies for crop cultivar deployment on disease dynamics, resistance durability and long-term evolutionary control, Evolutionary Applications, Volume 11 (2017) no. 5, pp. 705-717 | DOI

[56] Papaïx, J.; Touzeau, S.; Monod, H.; Lannou, C. Can epidemic control be achieved by altering landscape connectivity in agricultural systems?, Ecological Modelling, Volume 284 (2014), pp. 35-47 | DOI

[57] Pariaud, B.; Robert, C.; Goyeau, H.; Lannou, C. Aggressiveness Components and Adaptation to a Host Cultivar in Wheat Leaf Rust, Phytopathology, Volume 99 (2009) no. 7, pp. 869-878 | DOI

[58] Park, R. F. Breeding cereals for rust resistance in Australia, Plant Pathology, Volume 57 (2008) no. 4, pp. 591-602 | DOI

[59] Park, R. F.; Rees, R. G. Expression of adult plant resistance and its effect on the development of Puccinia striiformis f.sp. tritici in some Australian wheat cultivars, Plant Pathology, Volume 38 (1989) no. 2, pp. 200-208 | DOI

[60] Parlevliet, J. E. Components of Resistance that Reduce the Rate of Epidemic Development, Annual Review of Phytopathology, Volume 17 (1979) no. 1, pp. 203-222 | DOI

[61] Parlevliet, J. E. Euphytica, 124 (2002) no. 2, pp. 147-156 | DOI

[62] Pietravalle, S.; Lemarié, S.; van den Bosch, F. Durability of Resistance and Cost of Virulence, European Journal of Plant Pathology, Volume 114 (2006) no. 1, pp. 107-116 | DOI

[63] Pilet-Nayel, M.-L.; Moury, B.; Caffier, V.; Montarry, J.; Kerlan, M.-C.; Fournet, S.; Durel, C.-E.; Delourme, R. Quantitative Resistance to Plant Pathogens in Pyramiding Strategies for Durable Crop Protection, Frontiers in Plant Science, Volume 8 (2017) | DOI

[64] Poisot, T. Plant resistance to pathogens: just you wait?, Peer Community in Evolutionary Biology (2023) | DOI

[65] Qamar, M.; Gardezi, D. A.; Iqbal, M. Determination of Rust Resistance Gene Complex Lr34/Yr18 in Spring Wheat and its Effect on Components of Partial Resistance, Journal of Phytopathology, Volume 160 (2012) no. 11-12, pp. 628-636 | DOI

[66] Quan, W.; Hou, G.; Chen, J.; Du, Z.; Lin, F.; Guo, Y.; Liu, S.; Zhang, Z. Mapping of QTL lengthening the latent period of Puccinia striiformis in winter wheat at the tillering growth stage, European Journal of Plant Pathology, Volume 136 (2013) no. 4, pp. 715-727 | DOI

[67] Richardson, K. L.; Vales, M. I.; Kling, J. G.; Mundt, C. C.; Hayes, P. M. Pyramiding and dissecting disease resistance QTL to barley stripe rust, Theoretical and Applied Genetics, Volume 113 (2006) no. 3, pp. 485-495 | DOI

[68] Rimbaud, L.; Papaix, J.; Rey, J.-F.; Moury, B.; Barrett, L.; Thrall, P. Durable resistance or efficient disease control? Adult Plant Resistance (APR) at the heart of the dilemma [Dataset], Zenodo, 2023 | DOI

[69] Rimbaud, L.; Fabre, F.; Papaïx, J.; Moury, B.; Lannou, C.; Barrett, L. G.; Thrall, P. H. Models of Plant Resistance Deployment, Annual Review of Phytopathology, Volume 59 (2021) no. 1, pp. 125-152 | DOI

[70] Rimbaud, L.; Papaïx, J.; Barrett, L. G.; Burdon, J. J.; Thrall, P. H. Mosaics, mixtures, rotations or pyramiding: What is the optimal strategy to deploy major gene resistance?, Evolutionary Applications, Volume 11 (2018) no. 10, pp. 1791-1810 | DOI

[71] Rimbaud, L.; Papaïx, J.; Rey, J.-F. landsepi: Landscape Epidemiology and Evolution. R package version 1.1.1 , 2018 (https://cran.r-project.org/package=landsepi)

[72] Rimbaud, L.; Papaïx, J.; Rey, J.-F.; Barrett, L. G.; Thrall, P. H. Assessing the durability and efficiency of landscape-based strategies to deploy plant resistance to pathogens, PLOS Computational Biology, Volume 14 (2018) no. 4 | DOI

[73] Rime, D.; Robert, C.; Goyeau, H.; Lannou, C. Effect of host genotype on leaf rust (Puccinia triticina) lesion development and urediniospore production in wheat seedlings, Plant Pathology, Volume 54 (2005) no. 3, pp. 287-298 | DOI

[74] Sache, I.; Vallavieille-Pope, C. d. Classification of airborne plant pathogens based on sporulation and infection characteristics, Canadian Journal of Botany, Volume 73 (1995) no. 8, pp. 1186-1195 | DOI

[75] Sandoval-Islas, J. S.; Broers, L. H. M.; Mora-Aguilera, G.; Parlevliet, J. E.; Osada-Kawasoe, S.; Vivar, H. E. Quantitative resistance and its components in 16 barley cultivars to yellow rust, Puccinia striiformis f. sp. hordei, Euphytica, Volume 153 (2006) no. 3, pp. 295-308 | DOI

[76] Saubin, M.; Louet, C.; Bousset, L.; Fabre, F.; Frey, P.; Fudal, I.; Grognard, F.; Hamelin, F.; Mailleret, L.; Stoeckel, S.; Touzeau, S.; Petre, B.; Halkett, F. Improving sustainable crop protection using population genetics concepts, Molecular Ecology (2022) | DOI

[77] Smale, M.; Singh, R. P.; Sayre, K.; Pingali, P.; Rajaram, S.; Dubin, H. J. Estimating the Economic Impact of Breeding Nonspecific Resistance to Leaf Rust in Modern Bread Wheats, Plant Disease, Volume 82 (1998) no. 9, pp. 1055-1061 | DOI

[78] Sørensen, C. K.; Hovmøller, M. S.; Leconte, M.; Dedryver, F.; de Vallavieille-Pope, C. New Races of Puccinia striiformis Found in Europe Reveal Race Specificity of Long-Term Effective Adult Plant Resistance in Wheat, Phytopathology®, Volume 104 (2014) no. 10, pp. 1042-1051 | DOI

[79] Stuthman, D.; Leonard, K.; Miller‐Garvin, J. Breeding Crops for Durable Resistance to Disease, Advances in Agronomy, Elsevier, 2007, pp. 319-367 | DOI

[80] Suzuki, S. U.; Sasaki, A. How does the resistance threshold in spatially explicit epidemic dynamics depend on the basic reproductive ratio and spatial correlation of crop genotypes?, Journal of Theoretical Biology, Volume 276 (2011) no. 1, pp. 117-125 | DOI

[81] Taylor, P. D.; Fahrig, L.; Henein, K.; Merriam, G. Connectivity Is a Vital Element of Landscape Structure, Oikos, Volume 68 (1993) no. 3 | DOI

[82] Tomerlin, J. R. Temperature and Host Effects on Latent and Infectious Periods and on Urediniospore Production of Puccinia recondita f. sp. tritici, Phytopathology, Volume 73 (1983) no. 3 | DOI

[83] van den Bosch, F.; Gilligan, C. A. Measures of Durability of Resistance, Phytopathology, Volume 93 (2003) no. 5, pp. 616-625 | DOI

[84] Oijen, M. Selection and use of a mathematical model to evaluate components of resistance to Phytophthora infestans in potato, Netherlands Journal of Plant Pathology, Volume 98 (1992) no. 3, pp. 192-202 | DOI

[85] Watkinson-Powell, B.; Gilligan, C. A.; Cunniffe, N. J. When Does Spatial Diversification Usefully Maximize the Durability of Crop Disease Resistance?, Phytopathology, Volume 110 (2020) no. 11, pp. 1808-1820 | DOI

[86] Zhan, J.; Thrall, P. H.; Papaïx, J.; Xie, L.; Burdon, J. J. Playing on a Pathogen's Weakness: Using Evolution to Guide Sustainable Plant Disease Control Strategies, Annual Review of Phytopathology, Volume 53 (2015) no. 1, pp. 19-43 | DOI

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