Super-races are not likely to dominate a fungal population within a life time of a perennial crop plantation of cultivar mixtures: a simulation study
- Xiangming Xu
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Deployment of cultivars with different resistance in mixtures is one means to manage plant diseases and prolong the life of resistance genes. One major concern in adopting mixtures is the development of ‘super-races’ that can overcome many resistance genes present in the mixture. A stochastic simulation model was developed to study the dynamics of virulence alleles in two-cultivar mixtures of perennial crops, focusing on the effects of cost of virulence and pathogen reproduction mechanism. The simulated mechanism of virulence has characteristics of both major and minor genes.
Random genetic drift due to repeated population crashes during the overwintering phase led to fixation of a single fungal genotype (in terms of its virulence), often within 100 seasons. Overall, cost of virulence is most important in determining the virulence dynamics under the present model formulation. With cost of virulence incorporated, nearly all simulation runs ended up with a single fungal genotype that can infect only one of the two cultivars. In absence of cost of virulence, most of the simulation runs ended up with fungal genotypes that can infect both host cultivars but in many cases do not contain the maximum possible number of virulence alleles due to random drift. A minimum of 20% sexual reproduction between strains from different cultivars is necessary to ensure that the final fixed strains are able to infect both cultivars. Although the number of virulence alleles in the final genotype and the time to fixation are affected by simulation factors, most of the variability was among replicate simulation runs (i.e. stochastic in nature). The time to fixation is generally long relative to cropping cycles.
A single fungal genotype will dominate a population due to the bottleneck in overwintering with cost of virulence primarily determining whether the dominant genotype can infect both cultivars. However, the dominant genotype is unlikely to accumulate all the virulence alleles due to genetic drift. The risk of emergence and spread of super-races is insufficiently great to prevent the use of cultivar mixtures of perennial crops as a means to reduce disease development provided that host resistance structure in mixtures is altered every cropping cycle.
- Ye G-Y, Smith KF: Marker-assisted gene pyramiding for cultivar development. Plant Breeding Rev 2010, 33:219–256. CrossRef
- Mundt CC, Brophy LS: Influence of number of host genotype units on the effectiveness of host mixtures for disease control: a modeling approach. Phytopathology 1988, 78:1087–1094. CrossRef
- Lannou C, De Vallavieille-Pope C, Goyeau H: Host mixture efficacy in disease control: effects of lesion growth analyzed through computer-simulated epidemics. Plant Pathol 1994, 43:651–662. CrossRef
- Lannou C, De Vallavieille-Pope C, Goyeau H: Induced resistance in host mixtures and its effect on disease control in computer-simulated epidemics. Plant Pathol 1995, 44:478–489. CrossRef
- Xu X-M, Ridout MS: Stochastic simulation of the spread of race specific and non-specific aerial fungal pathogens in cultivar mixtures. Plant Pathol 2000, 49:207–218.
- Xu X-M: A simulation study on managing plant diseases by systematically altering spatial positions of cultivar mixture components between seasons. Plant Pathol 2011, 60:857–865. CrossRef
- Mundt CC, Browning JA: Genetic diversity and cereal rust management. In The Cereal Rusts Vol2, Disease, Distribution, Epidemiology, and Control. Edited by: Roelfs AP, Bushnell WR. Orlando: Academic Press, USA; 1985.
- Mundt CC, Brophy LS, Kolar SC: Effect of genotype unit number and spatial arrangement on severity of yellow rust in wheat cultivar mixtures. Plant Pathol 1996, 45:215–222. CrossRef
- Ntahimpera N, Dillard HR, Cobb AC, Seem RC: Anthracnose development in mixtures of resistant and susceptible dry bean cultivars. Phytopathology 1996, 86:668–673. CrossRef
- Frey KJ, Browning JA, Simons MD: Management systems for host genes to control disease loss. Ann N Y Acad Sci 1977, 287:1265–1267. CrossRef
- Didelot F, Brun L, Parisi L: Effects of cultivar mixtures on scab control in apple orchards. Plant Pathol 2007, 56:1014–1022. CrossRef
- Cox CM, Garrett KA, Bowden RL, Fritz AK, Dendy SP, Heer WF: Cultivar mixtures for the simultaneous management of multiple diseases: Tan spot and leaf rust of wheat. Phytopathology 2004, 94:961–969. CrossRef
- Mundt CC: Use of multiline cultivars and cultivar mixtures for disease management. Annu Rev Phytopathol 2002, 40:381–410. CrossRef
- Mundt CC: Importance of Autoinfection to the Epidemiology of Polycyclic Foliar Disease. Phytopathology 2009, 99:1116–1120. CrossRef
- Mundt CC, Sackett KE, Wallace LD: Landscape heterogeneity and disease spread: experimental approaches with a plant pathogen. Ecol Appl 2011, 21:321–328. CrossRef
- Villareal L, Lannou C: Selection for increased spore efficacy by host genetic background in a wheat powdery mildew population. Phytopathology 2000, 90:1300–1306. CrossRef
- Smithson JB, Lenne JM: Varietal mixtures: a viable strategy for sustainable productivity in subsistence agriculture. Ann Appl Biol 1996, 128:127–158. CrossRef
- Zhu YY, Chen HR, Fan JH, Wang YY, Li Y, Chen JB, Fan JX, Yang SS, Hu LP, Leung H, et al.: Genetic diversity and disease control in rice. Nature 2000, 406:718–722. CrossRef
- Lannou C, Hubert P, Gimeno C: Competition and interactions among stripe rust pathotypes in wheat-cultivar mixtures. Plant Pathol 2005, 54:699–712. CrossRef
- Lannou C: Intrapathotype diversity for aggressiveness and pathogen evolution in cultivar mixtures. Phytopathology 2001, 91:500–510. CrossRef
- Marshall B, Newton AC, Zhan J: Quantitative evolution of aggressiveness of powdery mildew under two-cultivar barley mixtures. Plant Pathol 2009, 58:378–388. CrossRef
- Brown JKM, Tellier A: Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu Rev Phytopathol 2011, 49:345–367. CrossRef
- Tellier A, Brown JKM: Stability of genetic polymorphism in host-parasite interactions. Proc R Soc B-Biological Sci 2007, 274:809–817. CrossRef
- Thrall PH, Burdon JJ: Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal. Plant Pathol 2002, 51:169–184. CrossRef
- Damgaard C: Coevolution of a plant host-pathogen gene-for-gene system in a metapopulation model without cost of resistance or cost of virulence. J Theor Biol 1999, 201:1–12. CrossRef
- Salathé M, Scherer A, Bonhoeffer S: Neutral drift and polymorphism in gene-for-gene systems. Ecology Letter 2005, 8:925–932. CrossRef
- Kirby GC, Burdon JJ: First: Effects of mutation and random drift on Leonard’s gene-for-gene coevolution model. Phytopathology 1997, 87:488–493. CrossRef
- Sasaki A: Host-parasite coevolution in a multilocus gene-for-gene system. Proc R Soc London, Ser B 2000, 267:2183–2188. CrossRef
- Leonard KJ: Modelling gene frequency dynamics. In The gene-for-gene relationship in plant-parasite interactions. Edited by: Crute IR, Holub EB, Burdon JJ. CAB International, Wallingford; 1997:211–230.
- Sapoukhina N, Durel C-E, Le Cam B: Spatial deployment of gene-for-gene resistance governs evolution and spread of pathogen populations. Theor Ecol 2009, 2:229–238. CrossRef
- Fabre F, Bruchou C, Palloix A, Moury B: Key determinants of resistance durability to plant viruses: Insights from a model linking within- and between-host dynamics. Virus Research 2009, 141:140–149. CrossRef
- Tellier A, Brown JKM: Polymorphism in multilocus host-parasite coevolutionary interactions. Genetics 2007, 177:1777–1790. CrossRef
- Tellier A, Brown JKM: Spatial heterogeneity, frequency-dependent selection and polymorphism in host-parasite interactions. BMC Evol Biol 2011, 11:319. CrossRef
- Barrett LG, Thrall PH, Burdon JJ, Nicotra AB, Linde CC: Population structure and diversity in sexual and asexual populations of the pathogenic fungus Melampsoralini. Mol Ecol 2008, 17:3401–3415. CrossRef
- Brown JKM: Recombination and selection in populations of plant-pathogens. Plant Pathol 1995, 44:279–293. CrossRef
- Bahri B, Leconte M, De Vallavieille-Pope C, Enjalbert J: Cost of virulence: Case of Puccinia striiformis f. sp tritici. Phytopathology 2007, 97:S6-S7.
- Huang Y-J, Balesdent M-H, Li Z-Q, Evans N, Rouxel T, Fitt BDL: Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeriamaculans (phoma stem canker of oilseed rape). Eur J Plant Pathol 2010, 126:279–291. CrossRef
- Montarry J, Hamelin FM, Glais I, Corbi R, Andrivon D: Fitness costs associated with unnecessary virulence factors and life history traits: evolutionary insights from the potato late blight pathogen Phytophthorainfestans. BMC Evol Biol 2010., 10:
- Burdon JJ, Thrall PH: Coevolution at multiple spatial scales: Linummarginale-Melampsora lini - from the individual to the species. Evol Ecol 2000, 14:261–281. CrossRef
- MacHardy WE: Apple scab: biology, epidemiology, and management. American Phytopathological Society, St. Paul, MN; 1996.
- Wellings C: Puccinia striiformis in Australia: a review of the incursion, evolution, and adaptation of stripe rust in the period 1979–2006. Aust J Agric Res 2007, 58:567–575. CrossRef
- Hennessy C, Walduck G, Daly A, Padovan A: Weed hosts of Fusariumoxysporum f. sp. cubense tropical race 4 in northern Australia. Australasian Plant Pathol 2005, 34:115–117. CrossRef
- Mollison D: Spatial contact models for ecological and epidemic spread. J R Stat Soc Series B 1977, 39:283–326.
- Xu X-M, Ridout MS: Effects of initial epidemic conditions, sporulation rate, and spore dispersal gradient on the spatio-temporal dynamics of plant disease epidemics. Phytopathology 1998, 88:1000–1012. CrossRef
- Shaw MW: Simulation of population expansion and spatial pattern when individual dispersal distributions do not decline exponentially with distance. Proc R Soc London, Ser B 1995, 259:243–248. CrossRef
- Barbara DJ, Roberts A, Xu X-M: Virulence characteristics of apple scab (Venturia inaequalis) isolates from monoculture and mixed orchards. Plant Pathol 2008, 57:552–561. CrossRef
- Wichmann BA, Hill ID: An efficient and portable pseudo-random number generator. Applied Statistics 1982, 31:188–190. CrossRef
- Payne RW (Ed): The guide to GenStat® release 9 - Part 2: Statistics. VSN International, Hemel Hempstead, UK; 2006.
- Super-races are not likely to dominate a fungal population within a life time of a perennial crop plantation of cultivar mixtures: a simulation study
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
- Online Date
- August 2012
- Online ISSN
- BioMed Central
- Additional Links
- Fungal diseases
- Super races
- Cost of virulence
- Mating system
- Xiangming Xu (1) (2)
- Author Affiliations
- 1. State Key Laboratory of Crop Stress Biology in Arid Areas, College of Plant Protection, Northwest A&F University, Yangling, 712100, China
- 2. East Malling Research, New Road, West Malling, Kent, ME19 6BJ, UK