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.     

Measures of durability of resistance

ABSTRACT Conventional models for the durability of resistant cultivars focus on the dynamics of the frequency of resistance genes. This leads to a definition of the durability of resistance as the time from introduction of the cultivar to the time when the frequency of the virulence gene reaches a preset threshold. It is questionable whether this is the most appropriate way to measure durability. Here we use a simple epidemiological model to link population dynamics and population genetics to compare three measures of durability: (i) the expected time until invasion of the virulent genotype, by mutation or immigration, and subsequent establishment of a population (T(invasion)); (ii) the virulence frequency related measure of the time for the virulent genotype to take-over the pathogen population ( T(take-over)); and (iii) the additional yield, measured by the additional number of uninfected host growth days (T(additional)). Specifically, we show how the measures of durability are affected by deployment and epidemiological parameters. We use a combination of numerical solution and analytical approximation of a model for the population dynamics of avirulent and virulent genotypes of a pathogen growing in dynamically changing populations of resistant and susceptible cultivars. The three measures of durability are compared. Some consequences of the results for durable resistance in multilines and mixtures and the regional deployment of resistant cultivars are discussed.     

Genetics of Virulence in Cochliobolus sativus and Resistance in Barley

ABSTRACT Spot blotch, caused by Cochliobolus sativus, is one of the most common foliar diseases of barley in the upper midwest region of the United States. To examine the genetics of host-specific virulence in C. sativus, a cross was made between isolate ND90Pr (which exhibits high virulence on barley genotype Bowman and low virulence on genotype ND 5883) and ND93-1 (which exhibits low virulence on both genotypes). Ascospore progeny segregated 48:55 for low virulence/high virulence on Bowman, indicating the presence of a single virulence gene in isolate ND90Pr. To complement the study of host-specific virulence in the pathogen, an experiment also was conducted on the genetics of specific resistance in the host. Progeny from a Bowman/ND 5883 cross were evaluated for their infection responses (IRs) to isolate ND90Pr at the seedling stage. The F(2) population segregated 1:3 for low IRs (resistant)/high IRs (susceptible), indicating the presence of a single resistance gene in genotype ND 5883. This result was confirmed in the F(3) generation, as a 1:2:1 ratio was found for homozygous resistant, segregating, and homozygous susceptible families, respectively. The data from this study demonstrate that both virulence in the pathogen and resistance in the host are under monogenic control in this specific host genotype/fungal isolate combination.     

Recombination and selection in populations of plant pathogens

A theoretical model has been used to study the dynamics of the frequencies of the following: a virulence gene which is selected by part of the host plant population; an unnecessary virulence gene, which is not required for infection of the host; and the gametic disequilibrium between the two genes. If the two genes are not initially in gametic equilibrium, the frequency of the unnecessary virulence may be altered greatly by hitch-hiking selection, because of the increased frequency of the selected virulence. The hitchhiking effect is strongest if reproduction is entirely asexual, but can still be significant if the frequency of recombination is less than the fraction of the host population which consists of selectively resistant plants. The frequency of recombination may be reduced if reproduction is partly clonal, rather than fully sexual, or if the two genes are linked. Selection against unnecessary virulence may give rise to complex dynamics of both virulence alleles; in particular, the frequency of an unnecessary virulence can rise substantially, by hitch-hiking selection, even if there is some sex or recombination. The direction in which the unnecessary virulence's frequency changes depends on the sign of the gametic disequilibrium between it and the selected gene, and on the existence of selection against unnecessary virulence. If there is no such selection, the long-term dynamics of genotype frequencies in a largely asexual pathogen population may be unpredictable. Consequently, disease control strategies based on planned replacements of one resistance gene by another are unlikely to be effective.     

Selection on Erysiphe graminis in pure and mixed stands of barley

The response of populations of Erysiphe graminis f. sp. hordei to selection by pure and mixed stands of three spring barley cultivars was studied in two field trials. The range of virulence of the pathogen genotypes selected in mixed host stands was dependent on the relative fitness of each genotype over all hosts. Unnecessary virulences were rapidly selected against on some hosts, but were less deleterious or favoured on others. In general there was selection for widely adapted pathogen genotypes in mixed host populations but this selection for flexibility limited the abilitytions in the absolute size of the pathogen population in host mixtures reduced the absolute frequencies of pathogen genotypes with combined virulences in comparison with those in pure stands. It is argued that host mixtures are therefore unlikely to favour rapid pathogen evolution towards races which are both widely adapted and highly virulent on all component cultivars which they can infect his definition docs not conform with conventional usage in population genetics.     

大豆花叶病毒(SMV)病显症率的模型预测

 大豆感染SMV系统量症前介体不能传毒。接种稀释10倍SMV病液显症率与介体传毒相似。介体和人工接种SMV于5个感病品种V₁-R₅ 9个生长时期共30余批次,结果表明SMV显症率主要决定于温度。显症起始温度为9℃,最适温度约26℃.V₁-R₂时期的植株显症所需有效积温基本一致;R₃-R₅时期比前者略有增加。累积显症率与累积有效积温的相关点图呈"S"型曲线分布,通过Weibull和Gompertz等8组曲线拟合选出拟合最优模型。V₁-R₂时期显症预测Gompertz拟合最好,得预测式:PP₁₁=Exp[-103021.196×Exp(-0.1329TT₁)]R₃-R₅时期Weibull拟合最好,得预测式:PP₁₂=1-Exp{-[0.02222(TT₁-65)^2.581]}     

Influence of host diversity on development of epidemics: an evaluation and elaboration of mixture theory

ABSTRACT A spatiotemporal/integro-difference equation model was developed and utilized to study the progress of epidemics in spatially heterogeneous mixtures of susceptible and resistant host plants. The effects of different scales and patterns of host genotypes on the development of focal and general epidemics were investigated using potato late blight as a case study. Two different radial Laplace kernels and a two-dimensional Gaussian kernel were used for modeling the dispersal of spores. An analytical expression for the apparent infection rate, r, in general epidemics was tested by comparison with dynamic simulations. A genotype connectivity parameter, q, was introduced into the formula for r. This parameter quantifies the probability of pathogen inoculum produced on a certain host genotype unit reaching the same or another unit of the same genotype. The analytical expression for the apparent infection rate provided accurate predictions of realized r in the simulations of general epidemics. The relationship between r and the radial velocity of focus expansion, c, in focal epidemics, was linear in accordance with theory for homogeneous genotype mixtures. The findings suggest that genotype mixtures that are effective in reducing general epidemics of Phytophthora infestans will likewise curtail focal epidemics and vice versa.     

葡萄与葡萄霜霉菌之间关系的研究水平系统学说

 利用15个葡萄霜霉菌的自然群体和5个抗性不同的寄主品种进行的特异性接种结果表明:病原自然群体间存在着致病力的差异;寄主品种间存在着抗病性的差异;但不存在寄主-病原间的特异互作。结果还表明:在特异品种上连读移种的情况下,虽然抗性品种能提高病原群体的致病力,但无寄主-病原间的特异性互作。据此提出了水平系统学说。如果这一学说得到证实,就可用欧洲葡萄品种间杂交来提高葡萄对霜霉病的抗性。     

Durability of Resistance and Cost of Virulence

A seasonal model, where a growing season is defined as the time between sowing and harvest and alternates with an inter-crop period, was derived to study the effects of the ‘cost of virulence’ and cropping ratio on durability of resistance. We assumed a single strain of virulent pathogen, a single strain of avirulent pathogen and two cultivars (one resistant and one susceptible) and studied two measures of durability of resistance (‘take-over time’ and ‘usefulness time’). Take-over time is defined as the time needed for the virulent strain of the pathogen to reach a preset threshold and predominate over the previous pathogen population. Usefulness time is the time needed before the estimated gain in green canopy area duration per plant through the use of the resistant cultivar becomes negligible. The model suggested that, although it could take several seasons before the virulent strain of the pathogen predominated over the previous pathogen population, the usefulness time of the resistant cultivar was always much shorter. Furthermore, increasing selection for the virulent strain of the pathogen (through increasing the cropping ratio of the resistant cultivar) caused the virulent strain of the pathogen to invade the system more rapidly. Cost of virulence, reflecting differences in pathogen infection rates between the four possible combinations of cultivar/pathogen strain, significantly affected durability of resistance, with the dynamics of the virulent and avirulent strains ranging from a case where the virulent strain of the pathogen died out to a case where the virulent strain of the pathogen invaded the resident pathogen population. An intermediate state, where the system reached equilibrium and the virulent strain of the pathogen neither became predominant nor died out, was defined as ‘coexistence’ of both strains of the pathogen. Occurrence of coexistence was directly related to the cost of virulence since it did not occur when virulence of the pathogen did not have a fitness cost. Two methods to include cost of virulence in the model gave similar results in relation to the two measures of durability of resistance studied.     

Intrapathotype diversity for aggressiveness and pathogen evolution in cultivar mixtures

ABSTRACT A model was developed and used to study the consequences of diversity for aggressiveness within pathotypes on pathogen evolution in two-component and four-component cultivar mixtures. It was assumed that, within a pathotype, a proportion of the isolates would have higher or lower spore efficacy than the average on a given host genetic background. Two situations were examined in which the pathogen can have either independent or negatively correlated values for spore efficacy on different cultivars. In the latter case, a pathogen genotype more aggressive than the average on a host genotype was always less aggressive on other host genotypes. In the simulations, isolates with greater aggressiveness relative to a host genotype were selected for and increased in frequency. However, because simple pathotypes always reproduced on the same host genotype whereas complex pathotypes were able to grow on several hosts, selection was faster for simple pathotypes. Pathotypes with two different levels of diversity for aggressiveness were compared with nondiversified pathotypes. In order to make comparisons, the effect of a 5 and 10% cost of virulence on the development of complex pathotypes was simulated. In general, increased diversity within pathotypes reduced the rate of increase of complex pathotypes in host mixtures, and this effect was stronger with greater frequencies of autodeposition of pathogen spores.     

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.     

Influence of spatial structure on pathogen colonization and extinction: a test using an experimental metapopulation

The Linum marginale–Melampsora lini plant–pathogen interaction has been studied extensively with regard to its epidemiology and population genetic structure (host resistance and pathogen virulence) in a natural metapopulation. In this study, this system was used in an experimental metapopulation approach to investigate explicitly how the distance (degree of isolation) between local population patches influences disease dynamics within a growing season, as well as the genetic structure of pathogen populations through stochastic colonization and extinction processes. The experimental design centred on four replicate sets of populations, within which patches were spaced at increasingly greater distances apart. Each patch consisted of an identical set of host and pathogen genotypes, with each pathogen genotype having the ability to attack only one of four host-resistance types. Over the 2 years of the experiment, the results showed clear 'boom-and-bust' epidemic patterns, with the strongest determinant of disease dynamics within a growing season being the identity of particular host–pathogen genotypic combinations. However, there were also significant effects of spatial structure, in that more isolated patches tended to exhibit lower levels of disease during epidemic peaks than patches that were close together. Extinction of pathogen genotypes from individual populations was positively related to the severity of disease during preceding epidemic peaks, but negatively related to the level of disease present at the final census prior to overwintering. The probability of recolonization of pathotypes into populations during the second growing season was most strongly related to the distance to the nearest neighbouring source population in which a given pathotype was present. Overall, these results highlight the importance of spatial scale in influencing the numerical and genetical dynamics of pathogen populations.     

Virulence Genes in Heterodera glycines: Allele Frequencies and Ror Gene Groups Among Field Isolates and Inbred Lines

ABSTRACT Genetic variation in field populations of Heterodera glycines is a key issue for both resistance gene deployment and basic understanding of virulence-gene flow in populations. In this study, we examined phenotypically defined genes for virulence under selection from host resistance. We separated the most common H. glycines genotypes in the United States into two virulence groups, based on their reproductive abilities on the resistant soybean plant introduction (PI) 88788. These groups correspond to previously identified virulence genes in the nematode, as follows: the dominant gene in H. glycines to PI88788, and the recessive genes to PI90763 and Pickett/Peking. Virulence allele frequencies and virulence genotype frequencies of selected field isolates were investigated by testing the host range of single-female-derived lines, which were developed through single-female inoculation on the standard susceptible soybean 'Lee 68'. By comparing virulence genotype frequencies between the original field isolates and their single-female-derived lines, we were able to determine allele frequencies in the field populations. The results suggest that tremendous variation in H. glycines virulence genes exists among field populations. Potential mechanisms of selection which could cause virulence genotype frequency increases are discussed as related to population genetics equilibrium theory.     

The dose rate debate: does the risk of fungicide resistance increase or decrease with dose?

This paper reviews the evidence relating to the question: does the risk of fungicide resistance increase or decrease with dose? The development of fungicide resistance progresses through three key phases. During the ‘emergence phase’ the resistant strain has to arise through mutation and invasion. During the subsequent ‘selection phase’, the resistant strain is present in the pathogen population and the fraction of the pathogen population carrying the resistance increases due to the selection pressure caused by the fungicide. During the final phase of ‘adjustment’, the dose or choice of fungicide may need to be changed to maintain effective control over a pathogen population where resistance has developed to intermediate levels. Emergence phase: no experimental publications and only one model study report on the emergence phase, and we conclude that work in this area is needed. Selection phase: all the published experimental work, and virtually all model studies, relate to the selection phase. Seven peer reviewed and four non‐peer reviewed publications report experimental evidence. All show increased selection for fungicide resistance with increased fungicide dose, except for one peer reviewed publication that does not detect any selection irrespective of dose and one conference proceedings publication which claims evidence for increased selection at a lower dose. In the mathematical models published, no evidence has been found that a lower dose could lead to a higher risk of fungicide resistance selection. We discuss areas of the dose rate debate that need further study. These include further work on pathogen‐fungicide combinations where the pathogen develops partial resistance to the fungicide and work on the emergence phase.     

Pathogenicity and infectivity of Phytophthora ramorum vary depending on host species,infected plant part,inoculum potential,pathogen genotype,and temperature

A total of 25 ornamental plant species representing 10 families were inoculated using three genotypes, each representing one of the genetic lineages NA1, NA2, and EU1 of the pathogen Phytophthora ramorum. Leaves were inoculated using suspensions with two zoospore concentrations and exposure at three temperatures, while stems were inoculated using agar plugs colonized by mycelia. Susceptibility was determined by measuring either the success of pathogen reisolation or lesion length caused by the pathogen. Infectivity was determined by counting sporangia in washes of inoculated leaves or stems. Results from all three pathogen genotypes combined were used to rank each of the 25 plant species for susceptibility and infectivity, while pooled results per genotype from all 25 hosts combined were employed for a preliminary comparison of pathogenicity and infectivity among genotypes. Statistical analyses showed that leaf results were affected by the concentration of zoospores, temperature, plant host, pathogen genotype, and by the interaction between host and pathogen genotype. Stem results were mostly affected by host and by the interaction between host and pathogen genotype. Hosts ranked differently when looking at the various parameters, and differences in rankings were also significant when comparing stem and leaf results. Differences were identified among the 25 hosts and the three pathogen genotypes for all parameters: results can be used for decision-making regarding regulations or selection of plants to be grown where infestations by P. ramorum are an issue.     

Evidence of early defence to Ascochyta lentis within the recently identified Lens orientalis resistance source ILWL180

In plant–pathogen interactions, strong structural and biochemical barriers may induce a cascade of reactions in planta, leading to host resistance. The kinetic speed and amplitudes of these defence mechanisms may discriminate resistance from susceptibility to necrotrophic fungi. The infection processes of two Ascochyta lentis isolates (FT13037 and F13082) on the recently identified ascochyta blight (AB)‐resistant Lens orientalis genotype ILWL180 and two cultivated genotypes, ILL7537 (resistant) and ILL6002 (susceptible), were assessed. Using histopathological methods, significant differences in early behaviour of the isolates and the subsequent differential defence responses of the hosts were revealed. Irrespective of virulence, both isolates had significantly lower germination, shorter germ tubes and delayed appressorium formation on the resistant genotypes (ILWL180 and ILL7537) compared to the susceptible genotype (ILL6002); furthermore, these were more pronounced on genotype ILWL180 than on genotype ILL7537. Subsequently, host perception of pathogen entry led to the faster accumulation and notably higher amounts of reactive oxygen species and phenolic compounds at the penetration sites of the resistance genotypes ILWL180 and ILL7537. In contrast, genotype ILL6002 responded slowly to the A. lentis infection and reaffirmed previous gross disease symptomology reports as highly susceptible. Interestingly, quantification of H₂O₂ was markedly higher in ILWL180 particularly at 12 h post‐inoculation compared to ILL7537, potentially indicative of its superior resistance capability. Faster recognition of A. lentis is likely to be a major contribution to the superior resistance observed in genotype ILWL180 to the highly aggressive isolates of A. lentis assessed.     

Small-scale fungicide spray heterogeneity and the coexistence of resistant and sensitive pathogen strains

ABSTRACT Empirical evidence indicates that fungicide-resistant and sensitive strains can coexist for prolonged periods. Coexistence has important practical implications, for example, for the posttreatment recovery of sensitivity and consequently the life expectancy of fungicide products. Despite this, the factors influencing coexistence remain relatively unexplored. Ecological studies have shown that environmental heterogeneity can facilitate the coexistence of different species and subspecific groups. Here we use a simple differential equation model and show that fungicide spray heterogeneity per se is not sufficient for coexistence but that the outcome depends crucially on the competitive relationship between resistant and sensitive strains. The model incorporates the competition between resistant and sensitive pathogen strains for a limited supply of susceptible host tissue on a crop which has received an incomplete coverage of fungicide. We use a combination of invasibility analysis and model simulations to explore the conditions under which coexistence can occur. We further show that the maximum density of healthy host tissue isrealized when resistant and sensitive pathogen strains coexist. A set of key influencing parameters are identified and analyzed, and the consequences of the results for disease and resistance management are discussed.     

菜豆锈病菌侵染对寄主超微结构的作用及菜豆抗锈病的细胞学表现

 在电镜下观察发现,菜豆锈病菌侵染菜豆后,逐步对其超微结构产生影响:寄主细胞发生质壁分离;叶绿体变形;叶绿体的片层结构排列零乱;线粒体脊模糊不清,直至叶绿体解体;线粒体空泡化;少数细胞的细胞壁分解;不同细胞的细胞器堆积在一起。同时,病原菌的侵染激发了寄主抗病性的细胞学表现:供试的抗感菜豆品种都表现为在病原菌侵入位点的寄主细胞壁内侧有高电子致密物质沉积;与吸器母细胞接触的寄主细胞壁加厚以及在吸器颈周围有电子不透明物质形成。只是这3种反应在抗病品种中表现得更加强烈。此外,抗病品种中还有一些特有的抗性特征,如被侵染细胞及其相邻细胞的快速坏死,吸器母细胞侵入位点的寄主细胞壁外侧也有一种高电子致密物质沉积,抗病品种中真菌吸器周围聚集含大量线粒体的寄主细胞的细胞质,且吸器外基质比感病品种中的宽。     

Effects of thiophanate-methyl and azoxystrobin on the composition of Cercospora kikuchii populations with thiophanate-methyl-resistant strains

Azoxystrobin was recently registered in Japan for the control of purple seed stain of soybean caused by Cercospora kikuchii, because the pathogen has developed resistance to thiophanate-methyl. To investigate the effects of these fungicides on the frequency of C. kikuchii strains resistant to thiophanate-methyl and on the genotype structure of the population, we sowed purple-stained seeds, approximately 40% of which were infected with resistant strains, as inocula with asymptomatic seeds and applied thiophanate-methyl and azoxystrobin during the reproductive growth of soybeans. The isolation frequency of resistant strains increased more than 99% by thiophanate-methyl but was not significantly increased by azoxystrobin. In amplified fragment length polymorphism (AFLP) DNA fingerprinting, genotypic diversity was significantly decreased by thiophanate-methyl but was not affected by azoxystrobin. In addition, the similarity of the AFLP genotype structure was increased by thiophanate-methyl but not by azoxystrobin. These results suggest that thiophanate-methyl selectively inhibited the proliferation of sensitive strains, which resulted in a small number of genotypes, most of which were resistant strains. Azoxystrobin was found to nonselectively inhibit proliferation of the pathogen, which retained a large number of genotypes including thiophanate-methyl-sensitive or thiophanate-methyl-resistant strains or both. The nucleotide sequence data for the cytochrome b gene are available in the DDBJ/EMBL/GenBank databases under accession number AB231863.     

The population dynamics of disease on short and long time-scales

Observational evidence is scarce concerning the distribution of plant pathogen population sizes or densities as a function of time-scale or spatial scale. For wild pathosystems we can only get indirect evidence from evolutionary patterns and the consequences of biological invasions. We have little or no evidence bearing on extermination of hosts by pathogens, or successful escape of a host from a pathogen. Evidence over the last couple of centuries from crops suggest that the abundance of particular pathogens in the spectrum affecting a given host can vary hugely on decadal time-scales. However, this may be an artefact of domestication and intensive cultivation. Host-pathogen dynamics can be formulated mathematically fairly easily–for example as SIR-type differential equation or difference equation models, and this has been the (successful) focus of recent work in crops. “Long-term” is then discussed in terms of the time taken to relax from a perturbation to the asymptotic state. However, both host and pathogen dynamics are driven by environmental factors as well as their mutual interactions, and both host and pathogen co-evolve, and evolve in response to external factors. We have virtually no information about the importance and natural role of higher trophic levels (hyperpathogens) and competitors, but they could also induce long-scale fluctuations in the abundance of pathogens on particular hosts. In wild pathosystems the host distribution cannot be modelled as either a uniform density or even a uniform distribution of fields (which could then be treated as individuals). Patterns of short-term density-dependence and the detail of host distribution are therefore critical to long-term dynamics. Host density distributions are not usually scale-free, but are rarely uniform or clearly structured on a single scale. In a (multiply structured) metapopulation with co-evolution and external disturbances it could well be the case that the time required to attain equilibrium (if it exists) based on conditions stable over a specified time-scale is longer than that time-scale. Alternatively, local equilibria may be reached fairly rapidly following perturbations but the meta-population equilibrium be attained very slowly. In either case, meta-stability on various time-scales is a more relevant than equilibrium concepts in explaining observed patterns.