Dynamics of primary and secondary infection in take-all epidemics

ABSTRACT Using a combination of experimentation and mathematical modeling, the effects of initial (particulate) inoculum density on the dynamics of disease resulting from primary and secondary infection of wheat by the take-all fungus, Gaeumannomyces graminis var. tritici, were tested. A relatively high inoculum density generated a disease progress curve that rose monotonically toward an asymptote. Reducing the initial inoculum density resulted in a curve that initially was monotonic, rising to a plateau, but which increased sigmoidally to an asymptotic level of disease thereafter. Changes in the infectivity of particulate inoculum over time were examined in a separate experiment. Using a model that incorporated terms for primary and secondary infection, inoculum decay, and host growth, we showed that both disease progress curves were consistent with consecutive phases dominated, respectively, by primary and secondary infection. We examined the spread of disease from a low particulate inoculum density on seminal and adventitious root systems separately. Although seminal roots were affected by consecutive phases of primary and secondary infection, adventitious roots were affected only by secondary infection. We showed that the characteristic features of disease progress in controlled experiments were consistent with field data from crops of winter wheat. We concluded that there is an initial phase of primary infection by G. graminis var. tritici on winter wheat as seminal roots grow through the soil and encounter inoculum, but the rate of primary infection slows progressively as inoculum decays. After the initial phase, there is an acceleration in the rate of secondary infection on both seminal and adventitious roots that is stimulated by the increase in the availability of infected tissue as a source of inoculum and the availability of susceptible tissue for infection.     

Genetic Structure of Heterobasidion annosum in White Fir Mortality Centers in California

ABSTRACT The structure of Heterobasidion annosum populations was studied in 15 mixed-conifer sites in central and northern California. Study sites displayed mortality of white fir trees in enlarging discrete patches (mortality centers). At each site, fungal genotypes were defined by somatic compatibility tests. In two sites, further genetic and molecular analyses were performed on field genotypes and on homokaryons obtained by dedikaryotization of field heterokaryons. Isolates were found to be colonizing mostly the roots and the bole sapwood of white fir trees, and no significant infections of other tree species were observed. Each mortality center was characterized by the presence of several fungal genotypes, all belonging to the S intersterility group. Both homokaryotic and heterokaryotic strains were present in all sites. Multiple genotypes were retrieved in individual trees or stumps. Out of 228 fungal genotypes, 86% were found only within a single tree or stump, while 14% had spread to adjacent trees. The two largest genotypes had diameters of 9 and 10 m, and had colonized five and nine trees, stumps, or both, respectively. The maximum distance between two adjacent trees colonized by the same genotype was 6 m, and a highly significant correlation was found between tree diameter and distance of fungal "vegetative" spread. The largest clones were found in areas characterized by high tree and stump densities, and secondary spread of the fungus was more significant in denser stands. In most cases, original infection courts of existing genotypes could be traced to standing trees and not to stumps. The genetic analysis performed in two mortality centers revealed that most local genotypes had different mating alleles, and thus originated from unrelated basidiospores. In a few cases, the same mating allele was shared by two heterokaryons (n+n genome) or by a homokaryon (n genome) and a heterokaryon. Molecular analysis showed that nuclei bearing the same mating allele were identical, providing evidence that the two nuclei forming heterokaryons can act independently in the field and can be shared among isolates, presumably via di-mon mating or by separate matings of different portions of widespread homokaryons.     

Epidemiology and chemical control of take-all on seminal and adventitious roots of wheat

ABSTRACT Epidemiological modeling is used to examine the effect of silthiofam seed treatment on field epidemics of take-all in winter wheat. A simple compartmental model, including terms for primary infection, secondary infection, root production, and decay of inoculum, was fitted to data describing change in the number of diseased and susceptible roots per plant over thermal time obtained from replicated field trials. This produced a composite curve describing change in the proportion of diseased roots over time that increased monotonically to an initial plateau and then increased exponentially thereafter. The shape of this curve was consistent with consecutive phases of primary and secondary infection. The seed treatment reduced the proportion of diseased roots throughout both phases of the epidemic. However, analysis with the model detected a significant reduction in the rate of primary, but not secondary, infection. The potential for silthiofam to affect secondary infection from diseased seminal or adventitious roots was examined in further detail by extending the compartmental model and fitting to change in the number of diseased and susceptible seminal or adventitious roots. Rates of secondary infection from either source of infected roots were not affected. Seed treatment controlled primary infection of seminal roots from particulate inoculum but not secondary infection from either seminal or adventitious roots. The reduction in disease for silthiofam-treated plants observed following the secondary infection phase of the epidemic was not due to long-term activity of the chemical but to the manifestation of disease control early in the epidemic.     

An Epidemiological Analysis of the Role of Disease-Induced Root Growth in the Differential Response of Two Cultivars of Winter Wheat to Infection by Gaeumannomyces graminis var. tritici

ABSTRACT Epidemiological modeling combined with parameter estimation of experimental data was used to examine differences in the contribution of disease-induced root production to the spread of take-all on plants of two representative yet contrasting cultivars of winter wheat, Ghengis and Savannah. A mechanistic model, including terms for primary infection, secondary infection, inoculum decay, and intrinsic and disease-induced root growth, was fitted to data describing changes in the numbers of infected and susceptible roots over time at a low or high density of inoculum. Disease progress curves were characterized by consecutive phases of primary and secondary infection. No differences in root growth were detected between cultivars in the absence of disease and root production continued for the duration of the experiment. However, significant differences in disease-induced root production were detected between Savannah and Genghis. In the presence of disease, root production for both cultivars was characterized by stimulation when few roots were infected and inhibition when many roots were infected. At low inoculum density, the transition from stimulation to inhibition occurred when an average of 5.0 and 9.0 roots were infected for Genghis and Savannah, respectively. At high inoculum density, the transition from stimulation to inhibition occurred when an average of 4.5 and 6.7 roots were infected for Genghis and Savannah, respectively. Differences in the rates of primary and secondary infection between Savannah and Genghis also were detected. At a low inoculum density, Genghis was marginally more resistant to secondary infection whereas, at a high density of inoculum, Savannah was marginally more resistant to primary infection. The combined effects of differences in disease-induced root growth and differences in the rates of primary and secondary infection meant that the period of stimulated root production was extended by 7 and 15 days for Savannah at a low and high inoculum density, respectively. The contribution of this form of epidemiological modeling to the better management of take-all is discussed.     

Fireweed (Epilobium angustifolium) as a possible inoculum reservoir for root-rotting Armillaria species

Two glasshouse experiments were conducted to determine the potential for Armillaria species to infect fireweed and subsequently use it as a food base for attacking lodgepole pine. Aspen segments colonized by A. mellea and A. ostoyae were used to inoculate fireweed roots. Both species caused infection, although the former was more pathogenic, attacking 28 of 42 inoculated fireweed roots as opposed to 8 of 60 in the case of the latter species. None of the nine pines inoculated with segments of fireweed roots colonized by A. ostoyae became infected, even though the isolates were pathogenic on pine when aspen segments were used as the food base. In contrast, 8 of 29 pine seedlings inoculated with fireweed colonized by A. mellea were killed, thus suggesting that fireweed could play some role in the epidemiology of this disease.     

Stock-Type Susceptibility and Delineation of Treatment Areas for a Cryptic Pinus radiata Root Disease

ABSTRACT Planting material with superior resistance to Armillaria root disease was identified in a field trial established to investigate variation in Armillaria infection among different Pinus radiata nursery stock types. At stand age 6.4 years, total infection incidence, mortality, and degree of root collar girdling by Armillaria spp. were all significantly lower among trees derived from both rooted stool bed cuttings (physiological age 1 to 3 years) and rooted field cuttings (physiological age 3 to 6 years) than among those grown from seedlings. Cutting types did not differ significantly from one another. No significant differences were found between stock types in stem diameter, but trees from stool bed cuttings were significantly taller than seedling trees. Whether these differences remain detectable later in the rotation, initial results suggest that it may be advantageous to plant robust stock, of either cuttings or seedlings, on Armillaria-infested sites. The incidence of infection in living, green-crowned trees was unevenly distributed across the trial site, and was greater nearer to trees killed by Armillaria spp. than further away (significant within a radius of 10 m). By mapping visible Armillaria-caused mortality prior to thinning, it may be possible to delineate areas with a higher incidence of concealed chronic infection, thus defining infested sites for postharvest treatment.     

Species of Armillaria in southern England

Isolates of Armillaria obtained from a wide variety of material were identified by means of the mating test devised by korhonen and by their growth on various media. Pathogenicity was tested by inoculating small pines. Five species were found, of which Armillaria mellea (Vahl ex Fr.) Kummer and A, ostoyae (Romagn.) Herink were highly pathogenic: the former killed a wide variety of broadleaved trees and conifers whilst the latter killed fewer species, mainly conifers. A. bulbosa [Armillariella bulbosa (Barla) Romagn.] was much less pathogenic and was found in trees weakened by suppression or in other ways;it also caused extensive butt-rot in some broad-leaved trees. A. tabescens (Scop, ex Fr.) Emel, was less common and occurred in stumps of broadleaved trees: it was virtually non-pathogenic. A species provisionally designated B by Korhonen was discovered only once. Brief accounts are given of these species with respect to rhizomorph behaviour and factors affecting their occurrence in woodland and gardens.     

Spread of Heterobasidion annosum in Christmas Tree Plantations of the United States Pacific Northwest

ABSTRACT The population structure of Heterobasidion annosum in the Pacific Northwest (PNW) Christmas tree plantations was estimated at two spatial scales to assess the relative importance of primary and secondary infection, colonization, and spread of the pathogen. Ninety-three isolates from single trees in 27 discrete mortality pockets and 104 isolates from 12 individual root systems of noble and Fraser fir trees were sampled near Mossyrock, Washington. Isolates were genotyped using somatic compatibility assays and microsatellite markers to determine the spatial scale at which dispersal of single genotypes (genets) was occurring. All isolates sampled from different trees in discrete mortality pockets had distinct genotypes, whereas the root systems of single trees were dominated by one or two genotypes. These results suggest that infection of PNW Christmas trees results from frequent primary infection events of adjacent stumps and localized secondary spread within root systems rather than clonal spread of the pathogen between adjacent trees. We hypothesize that mortality pockets may be due to availability of infection courts and/or variation in inoculum levels during selective harvesting of patches of mature trees.     

Effect and underlying mechanisms of pea-cereal intercropping on the epidemic development of ascochyta blight

Field experiments were conducted in western France for two consecutive years to investigate the effect of pea-cereal intercropping on ascochyta blight, a major constraint of field pea production world-wide. Disease pressure was variable in the experiments. Intercropping had almost no effect on disease development on stipules regardless of disease pressure. In contrast, disease severity on pods and stems was substantially reduced in the pea-cereal intercrop compared to the pea monocrop when the epidemic was moderate to severe. Therefore, a pea-cereal intercrop could potentially limit direct yield loss and reduce the quantity of primary inoculum available for subsequent pea crops. Disease reduction was partially explained by a modification of the microclimate within the intercrop canopy, in particular, a reduction in leaf wetness duration during and after flowering. The effect of intercropping on splash dispersal of conidia was investigated under controlled conditions using a rainfall simulator. Total dispersal was reduced by 39 to 78% in pea-wheat canopies compared to pea canopies. These reductions were explained by a reduction in host plant density and a barrier or relay effect of the non-host plants.     

Long-term development of Heterobasidion annosum in basidiospore-infected Sitka spruce stumps

The extent of colonization by Heterobasidion annosum was measured in 1989 in Sitka spruce stumps that had been inoculated with basidiospores in 1981 and assessed for infection in 1983. Only stumps that had infection in the sapwood in 1983 contained the fungus in 1989. There was a significant positive correlation between the sapwood area colonized in 1983 and the total area colonized in 1989. Between 1983 and 1989, H. annosum spread within the body of stumps and into most primary roots. There were significant correlations between the stump area colonized in 1983 and 1989 and the percentage of stump and root volume colonized in 1989. Roots of 26 excavated stumps were in contact with an average of two roots on each of two living trees. Fourteen roots on eight living trees became infected, and H. annosum spread proximally an average of 126 cm into trees. We believe that this is the first report of the transfer of H. annosum from spruce stumps inoculated with basidiospores to adjacent live trees.     

Epidemiological studies on cercospora leaf spot of sugar beet

In the glasshouse, inoculation of sugar beet with Cercospora beticola followed by 16 h of high humidity produced visible disease only with at least four conidia per cm² of leaf area. Disease became more severe after increasing periods of high humidity in the range of 0–24 h. In the field, spraying plants with water enhanced disease spread from a focus. Disease progress curves were sigmoid. Apparent infection rate declined towards the end of the season, possibly because of high temperature. In approximate agreement with prediction, epidemic development was delayed when initial inoculum was reduced. Reduced infection, resulting from either reduced initial inoculum or delayed inoculation, decreased the adverse effect of disease on sugar yield.     

Modeling and analysis of disease-induced host growth in the epidemiology of take-all

ABSTRACT Epidemiological modeling, together with parameter estimation to experimental data, was used to examine the contribution of disease-induced root growth to the spread of take-all in wheat. Production of roots from plants grown in the absence of disease was compared with production of those grown in the presence of disease and the precise form of diseaseinduced growth was examined by fitting a mechanistic model to data describing change in the number of infected and susceptible roots over time from a low and a high density of inoculum. During the early phase of the epidemic, diseased plants produced more roots than their noninfected counterparts. However, as the epidemic progressed, the rate of root production for infected plants slowed so that by the end of the epidemic, and depending on inoculum density, infected plants had fewer roots than uninfected plants. The dynamical change in the numbers of infected and susceptible roots over time could only be explained by the mechanistic model when allowance was made for disease-induced root growth. Analysis of the effect of disease-induced root production on the spread of disease using the model suggests that additional roots produced early in the epidemic serve only to reduce the proportion of diseased roots. However, as the epidemic switches from primary to secondary infection, these roots perform an active role in the transmission of disease. Some consequence of disease-induced root growth for field epidemics is discussed.     

Population Dynamics of Fusarium Oxysporum f. Sp. Radicis-lycopersici in Relation to the Onset of Fusarium Crown and Root Rot of Tomato

Fusarium oxysporum f. sp. radicis-lycopersici the causal agent of crown and root rot in tomato comprises two overlapping separate phases: monocyclic and polycyclic. Oversummering inoculum is the source of primary infection (the monocyclic phase) and the spread from plant to plant via root-to-root contact is the source of the secondary infection (the polycyclic phase). In the present work, relationships between initial inoculum density, population dynamics of the pathogen in the root zone of diseased plants, and disease onset were studied. For the monocyclic phase, 55.1% of the variance of disease onset was attributed to the rate of pathogen proliferation in the root zone of plants, and only 12.8% of the variance was attributed to the amount of initial inoculum density. For the polycyclic phase, disease onset was not related to either initial inoculum density or the rate of pathogen proliferation in the root zone. At disease onset, the inoculum density of the pathogen in the root zone of plants infected from oversummering inoculum reached an average of 4.08 log cfu g soil^–1. The inoculum density of the pathogen in the root zone of plants infected by their diseased neighbors was 3.23 log cfu g soil^–1. A large variation in pathogen proliferation rate in the root zone was found among individual plants, suggesting that differences in the level of soil suppressiveness may occur not only between fields, but even in the same field over short distances.     

Temporal and spatial aspects of the epidemiology of sorghum downy mildew on maize

The development of systemic disease from primary inoculum sources of sorghum downy mildew was studied on field-grown maize in Thailand. Data were recorded five times, from the first appearance of disease until 5 weeks after plant emergence. The incidence of diseased plants decreased with increasing distance from the primary inoculum sources, and the slope of the gradient flattened as the epidemic progressed. The steepest gradient of disease incidence was observed downwind. The progress in time and spread in space of disease about primary foci is described by three non-linear models which fit the data equally well. However, the resulting gradients at wider distances are different. With two models the gradients decrease asymptotically to zero with increasing distance, whilst the other model leads to negative values above a certain distance. The rates of isopath movement of all models decrease with time, but the effect of distance on the isopathic rate is different; the rate can decrease, stay constant or increase with distance.     

Interaction between Diplodia pinea and D. scrobiculata in red and jack pine seedlings

Sphaeropsis sapinea sensu lato is a conifer fungal pathogen that causes shoot blight and stem cankers. Recently, the former S. sapinea has been divided into two species, Diplodia pinea and D. scrobiculata. The aims of the study were to determine the contribution of each species in disease development on red and jack pines by means of co-inoculations and molecular identifications, and to evaluate how the presence of each species affects the development and aggressiveness of the other. Symptom severity (distance below the inoculation site at which necrotic needles were observed) and identification length (the maximum distance from inoculation site from which either D. pinea or D. scrobiculata was identified using molecular methods) were recorded 4 weeks after inoculating wounded seedlings with agar plugs colonized by these pathogens. The results suggested that D. pinea was much more aggressive on both hosts than D. scrobiculata. When a seedling was co-inoculated with these pathogens, the symptom development appeared to be mainly due to D. pinea. The presence of D. pinea also interfered with the establishment of D. scrobiculata in the plant tissue. However, D. scrobiculata showed antagonism toward D. pinea. When both pathogens co-occurred in a single seedling, symptom severity caused by D. pinea was less than when D. pinea alone was present.     

Disease-weather relationships for powdery mildew and yellow rust on winter wheat

Key weather factors determining the occurrence and severity of powdery mildew and yellow rust epidemics on winter wheat were identified. Empirical models were formulated to qualitatively predict a damaging epidemic (>5% severity) and quantitatively predict the disease severity given a damaging epidemic occurred. The disease data used was from field experiments at 12 locations in the UK covering the period from 1994 to 2002 with matching data from weather stations within a 5 km range. Wind in December to February was the most influential factor for a damaging epidemic of powdery mildew. Disease severity was best identified by a model with temperature, humidity, and rain in April to June. For yellow rust, the temperature in February to June was the most influential factor for a damaging epidemic as well as for disease severity. The qualitative models identified favorable circumstances for damaging epidemics, but damaging epidemics did not always occur in such circumstances, probably due to other factors such as the availability of initial inoculum and cultivar resistance.     

Disease Progression by Active Mycelial Growth and Biocontrol of Pythium ultimum var. ultimum Studied Using a Rhizobox System

ABSTRACT This study demonstrates that outward growth of mycelium from primary foci through bulk potting mix to roots of adjoining plants can be an important means of spread of damping-off and root rot caused by Pythium ultimum. The use of a rhizobox system, which confines plant roots, enabled us to study the spread of actively growing mycelium between root systems placed at precise distances from each other. In steamed potting mix, hyphae of P. ultimum on average grew 9.6 cm from diseased root tissue compared to 5.3 cm in raw potting mix. The density of mycelium was highest within the first 2 cm from the infected root tissue, decreasing with increasing distances from the roots. Accordingly, the disease on adjacent plants decreased as the distance from infected roots increased. The time required for damping-off of adjacent plants was 3 days slower in raw as compared to steamed potting mix and increased by 2 days for each additional centimeter between the rhizoboxes. The presence of Trichoderma harzianum diminished the production of secondary inoculum and reduced the ability of P. ultimum hyphae to extend through bulk potting mix. In conclusion, the concentration of the primary inoculum, the plant density, the distance separating diseased from healthy roots, the resident microflora, and the presence of an antagonist were shown to be important factors affecting disease spread by mycelial growth.     

接种体密度、土壤水分基质势和土壤温度对辣椒疫病死苗率的影响

 在生长箱内控制条件下分析测定了接种体密度、土壤水分基质势和土壤温度对辣椒疫病死苗率的影响。结果表明,在每克干土中接种1个辣椒疫霉菌孢子囊就能造成侵染,引致辣椒死苗,随着接种体密度升高死苗率增大,直至接种体孢子囊密度达到50~80个/g干土时死苗率达到最高。土壤温度和土壤水分状况是决定辣椒疫病死苗率的重要因子,病菌侵染的最适土温是22~28℃,土壤水分接近饱和,即土壤水分基质势(Ψ_m值)为0时最容易侵染发病,土壤过于干燥和过饱和都不利于侵染发病。辣椒疫病死苗率与土壤温度、土壤水分基质势及其互作之间可用数学模式描述。     

Influence of Temperature and Inoculum Density of Fusarium oxysporum f. sp. ciceris on Suppression of Fusarium Wilt of Chickpea by Rhizosphere Bacteria

The effects of temperature and inoculum density of Fusarium oxysporum f. sp. ciceris race 5 on suppression of Fusarium wilt in chickpea (Cicer arietinum) cv. PV 61 by seed and soil treatments with rhizobacteria isolated from the chickpea rhizosphere were studied in a model system. Disease development over a range of temperatures (20, 25, and 30 degrees C) and inoculum densities (25 to 1,000 chlamydospores per gram of soil) was described by the Gompertz model. The Gompertz relative rate of disease progress and final amount of disease increased exponentially and monomolecularly, respectively, with increasing inoculum densities. Disease development was greater at 25 degrees C compared with 20 and 30 degrees C. At 20 and 30 degrees C, disease development was greater at 250 to 1,000 chlamydospores per gram of soil compared with 25 to 100 chlamydospores per gram of soil. At 25 degrees C, increasing inoculum densities of the pathogen did not influence disease. Nineteen Bacillus, Paenibacillus, Pseudomonas, and Stenotrophomonas spp. out of 23 bacterial isolates tested inhibited F. oxysporum f. sp. ciceris in vitro. Pseudomonas fluorescens RGAF 19 and RG 26, which did not inhibit the pathogen, showed the greatest Fusarium wilt suppression. Disease was suppressed only at 20 or 30 degrees C and at inoculum densities below 250 chlamydospores per gram of soil. Bacterial treatments increased the time to initial symptoms, reduced the Gompertz relative rate of disease progress, and reduced the overall amount of disease developed.