Stable Polymorphisms in a Two-Locus Gene-for-Gene System

ABSTRACT A two-locus gene-for-gene model is presented to analyze coevolutionary dynamics in interactions between host plants and their pathogens. Using both analytical and simulation approximations, we show that the behavior of the model is very simple with one locus. In the reciprocal genetic feedback version, there is a smooth outward spiral toward the boundaries. In the delayed feedback version, there is an infinite family of closed curves corresponding to different initial conditions. Both versions of the model are stabilized by the addition of recurrent mutation. Either a stable interior equilibrium or a stable limit cycle appears. But with the two-locus model, different coevolutionary outcomes are predicted according to the parameter values. For a wide range of small and medium values of virulence and resistance costs, complex fluctuations arise. The number of virulence alleles per isolate and the number of resistance alleles per plant cycle indefinitely. If the costs of both virulence and resistance are above a threshold, the final state of the coevolutionary dynamics is a stable single-resistance static polymorphism in the host and avirulence in the parasite. An equivalent threshold to maintain a disease-free host population was obtained analytically for a multilocus system. These expressions can be used to determine the number of single-resistance host genotypes that would have to be present in a mixture to prevent the spread of any virulent race of pathogen. The model demonstrates that it is preferable to use mixtures of single-resistant genotypes rather than using multiple resistance alleles in the same cultivar.     

Two‐component cultivar mixtures reduce rice blast epidemics in an upland agrosystem

The effect of two‐component rice cultivar mixtures on the control of rice blast disease was studied in three different experiments under rainfed upland conditions in the Madagascar Highlands. The mixtures involved a susceptible cultivar (either susceptible or very susceptible) and a resistant cultivar in different mixture arrangements (random or row mixtures) and with different proportions of the susceptible cultivar (50, 20 and 16·7%), which were compared to the susceptible cultivar grown in a pure stand. The effect of these mixtures on the incidence and severity of leaf and panicle blast was measured weekly, and on yield and yield components at harvest time. The mixture effect was more efficient in reducing disease with a proportion of 16·7% susceptible component than with a proportion of 50%. Blast epidemic was significantly reduced in all three experiments. However, under high blast pressure, there was no reduction in the disease by the end of the epidemic and yields of the susceptible cultivar were almost zero whatever the mixture. In two other experiments performed under lower blast pressure, disease incidence and severity were significantly lower in mixtures, and yields of the susceptible cultivars grown in mixtures were higher than those of their respective pure stands. Cultivar mixtures are a promising strategy that could contribute to a more sustainable cultivation of rice under upland conditions in the context of subsistence agriculture in Madagascar, where all cropping operations are manual.     

A simulation study on managing plant diseases by systematically altering spatial positions of cultivar mixture components between seasons

A simulation study was conducted to investigate epidemic development of a race‐specific pathogen in cultivar mixtures over six consecutive seasons where the spatial position of each mixture component was systematically altered between seasons. Results showed that, even for a relative large genotype unit area in a mixture, altering cultivar positions between seasons could, on average, increase disease suppression by a third over the corresponding mixture without position changes between seasons. Overall, the disease suppression achieved by mixtures with position change between seasons was close to that achieved by random mixtures. Greater redistribution distance of overwintered inoculum reduced the disease control efficacy achieved by change in the position of individual mixture components between seasons. It is therefore concluded that using mixtures with a relatively large genotype unit area together with systematic changes in the spatial positions of individual mixture components between seasons is a feasible option for integrated disease management.     

Diversity and Complexity of Erysiphe graminis f.sp. hordei Collected from Barley Cultivar Mixtures or Barley Plots Treated with a Resistance Elicitor

Powdery mildew populations were analysed to determine the effects of a resistance elicitor and cultivar mixtures on genetic complexity and diversity. Isolations were made from a range of spring barley monocultures and mixtures in a field trial, and characterised for virulence and RAPD profile. In a second trial, isolates were taken from a single mixture from untreated and resistance elicitor-treated areas and from the components of the mixture in monoculture. The mildew population was not only highly heterogeneous for virulence characteristics, but also proved heterogeneous within pathotypes for molecular markers, indicating the major impact of sexual recombination on population structure and the lack of clonal dominance. Various diversity measurements were compared and the value of dissimilarity measurement for revealing genetic distance within a population was highlighted. There was a trend towards increasing complexity as the season progressed, but there was no consistent relationship between cultivar or mixture, disease control treatment, fertiliser treatment, replicate or position in trial, and pathogen genotype. Whilst the resistance elicitor did reduce mildew by 78% in the first trial, and there was no interaction with fertiliser level in its expression, control was substantially less in the second trial. There were no differences between mildew isolates from elicitor and control treatments. It was felt that more effective and consistent resistance elicitors need to be developed before it can be stated that they are unlikely to be eroded by selecting resistant or adapted mildew genotypes.     

Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal

The concept of gene-for-gene coevolution is a major model for research on disease resistance in crop plants. However, few theoretical or empirical studies have examined such systems in natural situations, and as a consequence, there is little knowledge of how spatial effects are likely to influence the evolution of host resistance and pathogen virulence in gene-for-gene interactions. In this work, a simulation approach was used to investigate the epidemiological and genetic consequences of varying host and pathogen dispersal in metapopulation situations. The results demonstrate clear impacts of dispersal distance on the total number of host and pathogen genotypes that are maintained, as well as on genetic variation at individual host resistance and pathogen virulence loci. Several other important results also emerged from this study. In contrast to the predictions of many earlier nonspatial models, so-called 'super-races' of pathogens do not always evolve and dominate, indicating that it is not necessary to assume costs of resistance or virulence to maintain high levels of polymorphism in biologically realistic situations. The rate of evolution of both resistance and virulence depend on the scale of dispersal, with greater mixing (as a function of dispersal scale) resulting in a faster approach to a dynamic endpoint. The model in this paper also predicts that, despite the greater total genotypic diversity of pathogens across the metapopulation, variation in host resistance will generally be greater than variation in pathogen virulence within local populations.     

Development of natural late blight epidemics in pure and mixed plots of potato cultivars with different levels of partial resistance

Late blight, caused by Phytophthora infestans , is the most severe disease of potato worldwide. Controlling late blight epidemics is difficult, and resistance of host cultivars is either not effective enough, or too easily overcome by the pathogen to be used alone. In field trials conducted for 3 years under natural epidemics, late blight severity was significantly lower in a susceptible cultivar growing in rows alternating with partially resistant cultivars (mixtures) than in unmixed plots of the susceptible cultivar alone. Partially resistant cultivars behaved similarly in unmixed and mixed plots. Mixtures of cultivars reduced disease progress rates and sometimes delayed disease onset over unmixed plots, but did so significantly only for the slowest epidemic. This suggests that reduction of area under the disease progress curve (AUDPC) in mixtures resulted from the cumulative action of minor effects. Disease distribution was focal in all plots at all dates, as shown by Morisita's index values significantly exceeding 1. Significant yield increases for the susceptible cultivar, and occasionally for the partially resistant ones, were observed in mixed-cultivar plots compared with single-cultivar plots. These results show that cultivar mixtures can significantly reduce natural, polycyclic epidemics in broadleaved plants attacked by pathogens causing rapidly expanding lesions.     

Competition and interactions among stripe rust pathotypes in wheat-cultivar mixtures

A series of experiments was conducted with wheat stripe rust to analyse competition between simple and complex pathotypes in host mixtures. Two different pathotype combinations were tested, with different host components. Each combination included a complex (able to infect two host components) and two simple pathotypes. For one of the combinations, induced resistance was tested in a separate experiment as a possible interaction among pathotypes. Disease severity and pathotype frequencies were measured three times during the epidemic, on each host component grown in pure stands and in mixtures. In one of the experiments, pathotype frequencies were also measured within secondary foci. One of the complex pathotypes appeared to have a low fitness on one of the host components and did not significantly increase in frequency in host mixtures relative to pure stands. The average frequency of the other complex pathotype increased during the first epidemic cycles, but remained stable afterwards, below expected values. The results suggest that the development of complex pathotypes in host mixtures may be influenced by differential aggressiveness on the host components, by induced resistance and by random effects resulting from the formation of disease foci, and depends on pathogen autoinfection rate and dispersal mechanisms.     

Epidemiology in mixed host populations

ABSTRACT Although plant disease epidemiology has focused on populations in which all host plants have the same genotype, mixtures of host genotypes are more typical of natural populations and offer promising options for deployment of resistance genes in agriculture. In this review, we discuss Leonard's classic model of the effects of host genotype diversity on disease and its predictions of disease level based on the proportion of susceptible host tissue. As a refinement to Leonard's model, the spatial structure of host and pathogen population can be taken into account by considering factors such as autoinfection, interaction between host size and pathogen dispersal gradients, lesion expansion, and host carrying capacity for disease. The genetic composition of the host population also can be taken into account by considering differences in race-specific resistance among host genotypes, compensation, plant competition, and competitive interactions among pathogen genotypes. The magnitude of host-diversity effects for particular host-pathogen systems can be predicted by considering how the inherent characteristics of a system causes it to differ from the assumptions of the classic model. Because of the limited number of studies comparing host-diversity effects in different systems, it is difficult at this point to make more than qualitative predictions. Environmental conditions and management decisions also influence host-diversity effects on disease through their effect on factors such as host density and epidemic length and intensity.     

Induced resistance in host mixtures and its effect on disease control in computer-simulated epidemics

The epidemic simulator EPIMUL was modified and used to study how induced resistance affected the development of epidemics in host mixtures. In the model, induced resistance resulted from the interaction of host tissue with avirulent spores and caused a reduction in the efficacy of virulent spores deposited afterwards. We denned three parameters to describe induced resistance: the level of protection, defined as the magnitude of reduction in the virulent spore efficacy for infecting host tissue; the host surface area protected by an interaction with one avirulent spore; and the duration of protection of the host tissue, in days. In our simulations, induced resistance slowed the epidemics and gave better disease control in the mixtures, even if protection lasted for only 2 days. The disease reduction in the mixture attributable to induced resistance was approximately proportional to the level of protection. The effect of induced resistance increased as the protected area increased. Epidemics were virtually unaffected by induced resistance restricted to the infection site, but the effect of induced resistance initially increased rapidly as larger areas were protected. There was little further gain as the protected area increased from 2·6% to 26%. The influence of induced resistance was reduced when the interactions between virulent and avirulent pathogens were reduced.     

Effect of genotype unit number and spatial arrangement on severity of yellow rust in wheat cultivar mixtures

Pure stands of a yellow rust-susceptible wheat cultivar, pure stands of a resistant cultivar, and a 1 : 1 random mixture of resistant and susceptible cultivars were compared to populations in which strips or hills of the cultivars were alternated to attain genotype units (units of the same host genotype) that were larger in area than that of a single wheat plant. These four host populations were grown in plots of different sizes in order also to alter the number of units per host population. The goal was to determine if increasing the number of genotype units in mixed populations of large genotype units improved disease control relative to pure-line populations by increasing the amount of inoculum exchange among genotype units. Random mixtures of the two cultivars always provided better disease control than did alternating strips or hills. Evidence for an effect of genotype unit number on the efficacy of mixtures for rust control was found in only one of three experiments. Random mixtures of the two cultivars increased grain yield relative to the pure stand mean, but alternating strips did not.     

The effect of component number on Rhynchosporium secalis infection and yield in mixtures of winter barley cultivars

Mixtures of winter barley cultivars containing up to six components were grown over three years with and without fungicide treatment. Yield increases were recorded for mixtures compared with the mean of their monoculture components and there was a significant trend towards greater benefit from increased number of components. These benefits were partially attributable to a corresponding increase in control of Rhynchosporium secalis as component number increased. The potential for exploitation of mixtures in cereals for control of splash-dispersed pathogens is discussed.     

Ecological Genomics and Epidemiology

The huge amount of genomic data now becoming available offers both opportunities and challenges for epidemiologists. In this “preview” of likely developments as the field of ecological genomics evolves and merges with epidemiology, we discuss how epidemiology can use new information about genetic sequences and gene expression to form predictions about epidemic features and outcomes and for understanding host resistance and pathogen evolution. DNA sequencing is now complete for some hosts and several pathogens. Microarrays make it possible to measure gene expression simultaneously for thousands of genes. These tools will contribute to plant disease epidemiology by providing information about which resistance or pathogenicity genes are present in individuals and populations, what genes other than those directly involved in resistance and virulence are important in epidemics, the role of the phenotypic status of hosts and pathogens, and the role of the status of the environmental metagenome. Conversely, models of group dynamics supplied by population biology and ecology may be used to interpret gene expression within individual organisms and in populations of organisms. Genomic tools have great potential for improving understanding of resistance gene evolution and the durability of resistance. For example, DNA sequence analysis can be used to evaluate whether an arms race model of co-evolution is supported. Finally, new genomic tools will make it possible to consider the landscape ecology of epidemics in terms of host resistance both as determined by genotype and as expressed in host phenotypes in response to the biotic and abiotic environment. Host phenotype mixtures can be modeled and evaluated, with epidemiological predictions based on phenotypic characteristics such as physiological age and status in terms of induced systemic resistance or systemic acquired resistance.     

Strategies for the Control of Fusarium Head Blight in Cereals

Fusarium head blight (FHB) is a widespread and destructive disease of small grained cereals caused by a number of Fusarium species and Microdochium nivale. In addition to causing significant reductions in grain yield, FHB can result in the reduction of grain quality, either by affecting grain processing qualities or by producing a range of toxic metabolites that have adverse effects on humans and livestock. Control of FHB can be achieved by a number of cultural, biological and chemical strategies along with the exploitation of host plant resistance. In recent years, much of the research undertaken for the control of FHB has been concentrated on understanding and exploiting the genetic resistance of cereal plants to FHB-causing pathogens. Although, a brief overview of genetic resistance is presented, this review seeks to summarise the significance of FHB and review the effectiveness of cultural, biological and chemical control strategies that have been investigated for the control the disease.     

Effect of wheat cultivar mixtures on populations of Puccinia striiformis races*

This study quantifies the frequency of simple and complex races (races that can infect two or more components) of Puccinia striiformis in mixtures of wheat cultivars possessing different race-specific resistance genes. Treatments were designed so that the complex race changed depending on the host mixture, thus enabling us to observe the influence of pathogen complexity in different genetic backgrounds. Six cultivar mixtures and one pure stand of winter wheat were inoculated with three races of P. striiformis at two locations for two seasons. Potted plants of three winter wheat cultivars, each susceptible to one of the three races of the pathogen, were used to sample the pathogen during the field epidemics. Disease incidence on the differential cultivars was used to calculate the proportion of the three races in each treatment. The specific cultivars included in the mixtures influenced the frequencies of the three races. Increasing the number of virulent races in a mixture reduced the frequency of the complex race relative to the other two races. The results suggest that genetic background of the pathogen race, host composition, and interaction among pathogen races may be as important as cost of virulence in determining race frequencies in mixtures.     

Quantitative evolution of aggressiveness of powdery mildew under two-cultivar barley mixtures

The effects of cultivar mixtures on the evolution of aggressiveness of barley powdery mildew ( Blumeria graminis f.sp . hordei ) were modelled. It was found that the rate and direction of evolution of pathogen aggressiveness in a race-non-specific system and value at equilibrium, depends on initial resistance levels, proportions of component cultivars, autodeposition rates, the relative magnitude of the benefit of autoinfection, and the cost of alloinfection of spores. In the model, mixing cultivars in any proportions tended to reduce the aggressiveness of pathogens at equilibrium compared with pure stands, but this effect decreased when two mixture components were extremely unbalanced in proportion. Under low and medium autodeposition rates, the best control of the evolution of the pathogen was achieved by mixing two components in roughly equal proportions. The magnitude of aggressiveness at equilibrium increased as autodeposition rates increased. Though the level of initial resistance of mixture components did not have an impact on the aggressiveness of pathogens at equilibrium, it strongly influenced the transient values of aggressiveness and therefore the total amount of disease caused over an evolutionary period. The cost to the pathogen of alloinfection and benefit of autoinfection per se did not affect the final level of aggressiveness, but did affect the time to reach equilibrium. However, the ratio of the cost to the benefit did influence the final aggressiveness of the pathogen.     

Resistance, epidemiology and sustainable management of Rhynchosporium secalis populations on barley

Rhynchosporium secalis is one of the most destructive pathogens of barley worldwide, causing yield decreases of up to 40% and reduced grain quality. Rhynchosporium is a polycyclic disease. Primary inoculum includes conidia produced on crop debris, infected seeds and possibly ascospores, although these have not yet been identified. Secondary disease spread is primarily by splash dispersal of conidia produced on infected leaves, which may be symptomless early in the growing season. Host resistance to R. secalis is mediated by both 'major' or host-specific genes (complete resistance) and 'minor' genes of smaller, generally additive effects (partial resistance). Crop growth stage and plant or canopy architecture can modify the expression of resistance. Resistance genes are distributed unevenly across the barley genome, with most being clustered on the short arms of chromosomes 1H, 3H, 6H and 7H, or in the centromeric region or on the long arm of chromosome 3H. Strategies used to manage rhynchosporium epidemics include cultivar resistance and fungicides, and also cultural practices such as crop rotation, cultivar mixtures and manipulation of sowing date, sowing rate or fertiliser rate. However, the high genetic variability of R. secalis can result in rapid adaptation of pathogen populations to render some of these control strategies ineffective when they are used alone. Sustainable control of rhynchosporium needs to integrate major-gene-mediated resistance, partial resistance and other strategies such as customized fungicide programmes, species or cultivar rotation, resistance gene deployment, clean seed and cultivar mixtures.     

Protective effects of a wheat cultivar mixture against splash‐dispersed septoria tritici blotch epidemics

The use of cultivar mixtures to control foliar fungal diseases is well documented for windborne diseases, but remains controversial for splash‐dispersed diseases. To try to improve this strategy, a cultivar mixture was designed consisting of two wheat cultivars with contrasted resistance to Mycosphaerella graminicola , responsible for the rainborne disease septoria tritici blotch (STB), in a 1:3 susceptible:resistant ratio rather than the 1:1 ratio commonly used in previous studies. The impact of natural STB epidemics in this cultivar mixture was studied in field experiments over 4 years. Weekly assessments of the number of sporulating lesions, pycnidial leaf area and green leaf area were carried out on the susceptible cultivar. In years with sufficient STB pressure, disease impacts on the susceptible cultivar in the mixture were always significantly lower than in the pure stand (e.g. 42% reduction of pycnidial leaf area for the three upper leaves in 2008 and 41% in 2009). In years with low STB pressure (2010 and 2011), a reduction of disease impacts was also shown but was not always significant. After major rainfall events, the number of sporulating lesions observed on the susceptible cultivar after one latent period was reduced on average by 45% in the mixture compared to the pure stand. All the measurements showed that a susceptible cultivar was consistently protected, at least moderately, in a mixture under low to moderate STB pressure. Therefore, the results prove that the design of an efficient cultivar mixture can include the control of STB, among other foliar diseases.     

Recent developments in the molecular discrimination of formae speciales of Fusarium oxysporum

Rapid and reliable detection and identification of potential plant pathogens is required for taking appropriate and timely disease management measures. For many microbial species of which all strains generally are plant pathogens on a known host range, this has become quite straightforward. However, for some fungal species this is quite a challenge. One of these is Fusarium oxysporum Schlechtend:Fr., which, as a species, has a very broad host range, while individual strains are usually highly host-specific. Moreover, many strains of this fungus are non-pathogenic soil inhabitants. Thus, with regard to effective disease management, identification below the species level is highly desirable. So far, the genetic basis of host specificity in F. oxysporum is poorly understood. Furthermore, strains that infect a particular plant species are not necessarily more closely related to each other than to strains that infect other hosts. Despite these difficulties, recently an increasing number of studies have reported the successful development of molecular markers to discriminate F. oxysporum strains below the species level.     

Two Properties of a Gene-for-Gene Coevolution System under Human Perturbations

ABSTRACT Recently, the gene-for-gene host-parasite coevolution model of Leonard was extended by incorporating two kinds of perturbations. The first kind was the natural perturbations that include those caused by pathogen migration between the two subpopulations of the host, forward and backward mutations in the host or pathogen populations, and some others. The second kind was human perturbations, such as constantly increasing the percentage of the resistant genotype within the host population each season. In this study, we quantitatively compared the two kinds of perturbations and extended the constantly changing human perturbation to include non-constant perturbations that are more likely to occur in the real world. Two properties of the modified Leonard model were revealed from this study. First, when both human perturbations and natural perturbations are involved, the effects of natural perturbations are very small compared with those of human perturbations. This finding ensures that, in the study of human perturbations, we can simplify the study by ignoring the effects of natural perturbations. Second, through the simulation of nonconstant perturbations, which assumes that the proportion of the resistant genotype of the host population increases over time, we found that the model reproduces the "boom and bust" epidemic cycles that are often found in agroecosystems.     

The spread oi Erysiphe graminis f. sp. hordei in mixtures of barley varieties

A model is proposed of mechanisms which might affect the progress of Erysiphe graminis f. sp. hordei in mixtures of barley varieties. Results obtained from two field trials indicate that the efffect of mixtures may be panitioned into three categoriesof the influence of the reduced density of the susceptible plants, the barrier effect of the resistant plants, and the induced resistance due to the non-virulent pathogen biotypes. In the early stages of plant growth the lower density of susceptible plants accounted for most of the reduction in pathogen development in mixtures. As the epidemic progressed, the barrier and induced resistance effects increased in importance and the total mixture effect was at a maximum mid-way through epidemic development. Towards the end of the trials the overall mixture effect declined though the influence of induced resistance was at its maximum. The reasons for these changes and their implications for the use of host varietal mixtures in disease control are discussed.
Mixtures also protected the crop against a pathogen other than the target organism.