Impacts of plant growth and architecture on pathogen processes and their consequences for epidemic behaviour

As any epidemic on plants is driven by the amount of susceptible tissue, and the distance between organs, any modification in the host population, whether quantitative or qualitative, can have an impact on the epidemic dynamics. In this paper we examine using examples described in the literature, the features of the host plant and the use of crop management which are likely to decrease diseases. We list the pathogen processes that can be affected by crop growth and architecture modifications and then determine how we can highlight the principal ones. In most cases, a reduction in plant growth combined with an increase in plant or crop porosity reduces infection efficiency and spore dispersal. Experimental approaches in semi-controlled conditions, with concomitant characterisation of the host, microclimate and disease, allow a better understanding and analysis of the processes impacted. Afterwards, the models able to measure and predict the effect of plant growth and architecture on epidemic behaviour are reviewed.     

Patterns of development of Septoria nodorum and S. tritici in some winter wheat crops in Western Europe, 1981-83

In data collected at 19 sites in Western Europe during 1981-83. two patterns of development of Septoria nodorum and S. tritici on foliage of winter wheal were distinguished. In sudden outbreaks, lesions appeared simultaneously on the upper leaf layers of crops, usually after the end of stem extension; these outbreaks were ascribed to short, heavy rain storms in which pycnidiospore inoculum in basal leaves was elevated up to 60 cm through the crop canopy. Gradual epidemics were characterized by disease arising on successive leaf layers as they appeared during sustained periods of weather suitable for inoculum transport and infection.
The data indicate incubation periods of 2-4 weeks for S. nodorum and 3-5 weeks for S. tritici. it is suggested that a leaf layer cannot normally sustain more than one pathogen generation and that its infection arises from inoculum borne on leaves older than in the layer situated immediately below it. The potential level of disease in a crop may relate to the amount of inoculum present in spring. The proportions of disease caused by the two Septoria species varied greatly between sites and years, but the data provided no explanation.
It is concluded that a septoria forecast scheme needs to recognise the importance of sudden disease outbreaks and to include not only weather but also host growth and inoculum factors.     

The effect of powdery mildew (Erysiphe graminis f. sp. hordei) and leaf rust (Puccinia hordei) on spring barley in New Zealand. II. Apical development and yield potential

Reduced yields caused by powdery mildew and leaf rust in two seasons were associated with reduced plant growth. Combinations of early, late and full epidemics in one season, and 12 epidemic combinations in the second, were designed to identify crop sensitivity to disease by comparing growth and development with healthy plants. Early epidemics reduced ear number by increasing tiller death, and reduced grain number by effects on spikelet, floret or grain abortion, depending on the type of epidemic. Epidemics later in crop growth increased floret and grain abortion and also reduced grain weight.
There was no compensation by later-determined components for reduced growth and delayed development at earlier growth stages. Plants infected at early growth stages were more sensitive to late infections, seen as effects on the later-determined components, than plants which were healthy initially. Interactions occurred between epidemics at different times and are likely to occur between diseases and other constraints.     

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.     

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.     

The role of seeds and airborne inoculum in the initiation of leaf blotch (Rhynchosporium secalis) epidemics in winter barley

Both airborne spores of Rhynchosporium secalis and seed infection have been implied as major sources of primary inoculum for barley leaf blotch (scald) epidemics in fields without previous history of barley cropping. However, little is known about their relative importance in the onset of disease. Results from both quantitative real‐time PCR and visual assessments indicated that seed infection was the main source of inoculum in the field trial conducted in this study. Glasshouse studies established that the pathogen can be transmitted from infected seeds into roots, shoots and leaves without causing symptoms. Plants in the field trial remained symptomless for approximately four months before symptoms were observed in the crop. Covering the crop during part of the growing season was shown to prevent pathogen growth, despite the use of infected seed, indicating that changes in the physiological condition of the plant and/or environmental conditions may trigger disease development. However, once the disease appeared in the field it quickly became uniform throughout the cropping area. Only small amounts of R. secalis DNA were measured in 24 h spore‐trap tape samples using PCR. Inoculum levels equivalent to spore concentrations between 30 and 60 spores per m³ of air were only detected on three occasions during the growing season. The temporal pattern and level of detection of R. secalis DNA in spore tape samples indicated that airborne inoculum was limited and most likely represented rain‐splashed conidia rather than putative ascospores.     

Host mixture efficacy in disease control: effects of lesion growth analyzed through computer-simulated epidemics

Lesion growth varies among foliar parasites and in order to study the effect of lesion growth on the efficacy of host mixtures to control epidemics, we altered the epidemic simulator Epimul by integrating a lesion growth function into the model. A theoretical study was performed by simulating epidemics caused by parasites with different lesion growth rates, spore dispersal gradients and multiplication rates. We found that increases in lesion growth rates resulted in large decreases in the effectiveness of mixtures for disease control and interacted strongly with parasite multiplication rate and spore dispersal gradient. The decline in mixture efficacy for epidemics with high lesion growth rates was reduced when parasite multiplication rate was higher and spore dispersal gradient steeper. Our results suggested that the lower number of infections on susceptible plants in the mixture as a result of inoculum loss on resistant hosts was partially compensated by lesion growth.     

Characterization of early leaf spot suppression by strip tillage in peanut

ABSTRACT Epidemics of early leaf spot of peanut (Arachis hypogaea), caused by Cercospora arachidicola, are less severe in strip-tilled than conventionally tilled fields. Experiments were carried out to characterize the effect of strip tillage on early leaf spot epidemics and identify the primary target of suppression using a comparative epidemiology approach. Leaf spot intensity was assessed weekly as percent incidence or with the Florida 1-to-10 severity scale in peanut plots that were conventionally or strip tilled. The logistic model, fit to disease progress data, was used to estimate initial disease (y(0)) and epidemic rate (r) parameters. Environmental variables, inoculum abundance, and field host resistance were assessed independently. For experiments combined, estimated y(0) was less in strip-tilled than conventionally tilled plots, and r was comparable. The epidemic was delayed in strip-tilled plots by an average of 5.7 and 11.7 days based on incidence and severity, respectively. Tillage did not consistently affect mean canopy temperature, relative humidity, or frequency of environmental records favorable for infection or spore dispersal. Host response to infection was not affected by tillage, but infections were detected earlier and at higher frequencies with noninoculated detached leaves from conventionally tilled plots. These data suggest that strip tillage delays early leaf spot epidemics due to fewer initial infections; most likely a consequence of less inoculum being dispersed to peanut leaves from overwintering stroma in the soil.     

A host-pathogen simulation model: powdery mildew of grapevine

An epidemiological model simulating the growth of a single grapevine stock coupled to the dispersal and disease dynamics of the airborne conidia of the powdery mildew pathogen Erysiphe necator was developed. The model input variables were either climatic (temperature, wind speed and direction) or related to the pathogen (location and onset of primary infection). The environmental input variables dictated plant growth and pathogen spread (latent period, infection, lesion growth, conidial spore production and release). Input parameters characterized the crop production system, the growth conditions and the epidemiological characteristics of the pathogen. Output described, at each time step, number, age and pattern of healthy and infected organs, infected and infectious leaf area and aerial density of spores released. Validation of the model was achieved by comparing model output with experimental data for epidemics initiated at different times of host growth. Epidemic behaviour for two contrasting years of crop development and 7 phenological stages at the time of primary infection (PI) was examined. For PI occurring at day 115 a vine with late budbreak (1998) showed 58% of primary leaves diseased at flowering compared with only 19% for a vine with early budbreak (2003). Depending on the phenological stage at PI (1–4 leaves), the proportion of diseased primary leaves decreased from 42% to 6% at flowering. Simulations suggested that differences resulted from the interplay between the timing of the first sporulation event, the phenological stage at the time of initial infection, and the age structure and spatial distribution of the leaf population.     

Effects of inoculum concentration, wetness duration and plant age on development of early blight (Alternaria solani) and on shedding of leaves in tomato plants

Effects of inoculum concentration, wetness duration and plant age on the development of tomato early blight were evaluated in relation to host susceptibility under controlled environmental conditions. The main effect of early blight was premature defoliation, which was linearly related to the percentage of leaf area showing symptoms. As ln(inoculum concentration, conidia mL⁻¹) increased from 6·2 to 11·5, the percentages of leaf area affected and of defoliation increased linearly. Four h of leaf wetness after inoculation were sufficient to initiate the disease on plants of hybrid Skala RZ but not on those of cv. Rio Rojo, for which at least 6 h leaf wetness were needed. As wetness duration increased up to 24 h, there was an increase in the percentage leaf area showing symptoms and in the percentage of defoliation, but thereafter there was no significant increase in either parameter. Tomato plants were susceptible to Alternaria solani at all growth stages, but susceptibility increased as plants matured. There were no significant differences in susceptibility between tomato cultivars and hybrids.     

Influence of crop growth and structure on the risk of epidemics by Mycosphaerella graminicola (Septoria tritici) in winter wheat

Generally, it is recognized that inocula of Septoria tritici present on the basal leaves of winter wheat crops are spread towards the top of the canopy by splashy rainfall. This mechanism of inoculum dispersal is commonly accepted to be a key limit on disease progression. Therefore, attempts to forecast epidemics of S. tritici often quantify rainfall by some means, but largely ignore measurement of pathogen and host variables. In the present study, we show that new wheat leaves emerge initially at a height below established leaves that can contain sporulating lesions of S. tritici . This presents the possibility of horizontal inoculum transfer, even without splashy rainfall. The extent and duration of overlap between emergent and established leaves was found to differ considerably with cultivar and sowing date. Nitrogen application had little effect on overlap, because differences in crop phenology, e.g. leaf area and nodal length, were relative. However, estimates of raindrop penetration to the base of crop canopies suggested that vertical movement of inoculum is affected by nitrogen application. Crops receiving more nitrogen are denser, and therefore less rainfall reaches the base of the canopy. The interactions between crop and pathogen development are discussed with reference to the implications for predicting disease risk. In particular, cultivar traits that promote disease escape are quantified.     

Current knowledge on plant/canopy architectural traits that reduce the expression and development of epidemics

To reduce the use of pesticides, innovative studies have been developed to introduce the plant as the centre of the crop protection system. The aim of this paper is to explain how architectural traits of plants and canopies induce a more or less severe epidemic and how they may be modified in order to reduce disease development. In particular, it focuses on three key questions: i) which processes linked to epidemics can be influenced by architecture ii) how can architecture be characterized relative to these modes of action, and iii) how can these effects be explored and exploited? The roles of plant/canopy architecture on inoculum interception, on epidemic development via the microclimate and on tissue receptivity are discussed. In addition, the concepts of disease avoidance, canopy porosity and an ideotype unfavourable for disease development are described. This paper shows that many advances have already been made, but progress is still required in four main fields: microclimatology, mathematical modelling of plants, molecular genetics and ideotype conception.     

Simulation of Potato Late Blight in the Andes. II: Validation of the LATEBLIGHT Model

ABSTRACT LATEBLIGHT, a mathematical model that simulates the effect of weather, host growth and resistance, and fungicide use on asexual development and growth of Phytophthora infestans on potato foliage, was validated for the Andes of Peru. Validation was needed due to recent modifications made to the model, and because the model had not been formally tested outside of New York State. Prior to validation, procedures to estimate the starting time of the epidemic, the amount of initial inoculum, and leaf wetness duration were developed. Observed data for validation were from field trials with three potato cultivars in the Peruvian locations of Comas and Huancayo in the department of Junín, and Oxapampa in the department of Pasco in 1999 and 2000 for a total of 12 epidemics. These data had not been used previously for estimating model parameters. Observed and simulated epidemics were compared graphically using disease progress curves and numerically using the area under the disease progress curve in a confidence interval test, an equivalence test, and an envelope of acceptance test. The level of agreement between observed and simulated epidemics was high, and the model was found to be valid according to subjective and objective performance criteria. The approach of measuring fitness components of potato cultivars infected with isolates of a certain clonal lineage of P. infestans under controlled conditions and then using the experimental results as parameters of LATEBLIGHT proved to be effective. Fungicide treatments were not considered in this study.     

A dynamic simulation model for powdery mildew epidemics on winter wheat*

A system dynamic model for epidemics of Blumeria graminis (powdery mildew) on wheat was elaborated, based on the interaction between stages of the disease cycle, weather conditions and host characteristics. The model simulates the progress of disease severity, expressed as a percentage of powdered leaf area, on individual leaves, with a time step of one day, as a result of two processes: the growth of fungal colonies already present on the leaves and the appearance of new colonies. By means of mathematical equations, air temperature, vapour pressure deficit, rainfall and wind are used to calculate incubation, latency and sporulation periods, the growth of pathogen colonies, infection and spore survival. Effects of host susceptibility to infection, and of leaf position within the plant canopy, are also included. Model validation was carried out by comparing model outputs with the dynamics of epidemics observed on winter wheat grown at several locations in northern Italy (1991–98). Simulations were performed using meteorological data measured in standard meteorological stations. As there was good agreement between model outputs and actual disease severity, the model can be considered a satisfactory simulator of the effect of environmental conditions on the progress of powdery mildew epidemics.     

Field studies of anthracnose symptoms and pathogen infection in different phases of the persimmon growing season

Anthracnose is the main disease of persimmon and is caused by Colletotrichum spp. The study of field epidemiology is essential for the development of efficient management of this disease. In this study, we investigated infection by Colletotrichum spp. throughout the persimmon growing season to understand the host–pathogen interactions better. We observed the production of primary inoculum of persimmon anthracnose and described how epidemics progress from secondary infections during the fruit crop season. The field study was carried out in an organic orchard with three susceptible persimmon cultivars, Fuyu, Kakimel and Jiro, for three consecutive seasons. Our results indicate that the pathogen survives in 1-year-old shoots, which are the sources of primary inoculum. Later that growing season, the inoculum reaches flowers and new shoots, developing symptoms and producing the secondary inoculum. Fruit drop was also observed, with or without symptoms of anthracnose, throughout the plant cycle. In some of the symptomless fruit, collected from the plant and from the ground where they had fallen, latent infections of Colletotrichum spp. were detected. Shoots, flowers, immature and ripened fruit remained infected throughout the growing season, producing conidia that could lead to new secondary infections within and among plants. The incidence of anthracnose in fruit at harvest and postharvest proved to be less relevant for disease management. Practices for chemical and cultural control of the disease throughout the persimmon growing season are discussed.     

Epidemics of Diaporthe adunca in experimental and in natural populations of Plantago lanceolata and the effect of partial resistance on disease development

Epidemics of the splash-dispersed pathogenic fungus Diaporthe adunca on its host, the perennial herb Plantago lanceolata , were followed during two consecutive years in transects at roadsides in the Netherlands. Epidemics of D. adunca were also studied on clones of a susceptible and a partially resistant genotype of P. lanceolata grown either in a pure stand or in a 1:1 mixture in small plots in the garden. The epidemics in the natural and experimental populations could be adequately described by logistic and Gompertz models, but large differences were found in final disease levels and relative growth rates. The effect of partial resistance on the epidemic in the mixture was less than in a pure stand, probably due to the provision of inoculum from the highly diseased susceptible genotype to the partially resistant genotype. In the garden focal and wind-direction effects were seen. In the natural populations the epidemics developed from numerous primary infected scapes making foci and wind-directions effects less conspicuous.     

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.     

Growth of leek rust epidemics in time in three cultivars during the early stage of the epidemic

The growth of leek rust epidemics in time under favourable conditions in three leek cultivars during two years was analysed. In both years, the highest disease levels were found on cultivar Albana, followed by Carina and Cortina. A simple model is presented to correct the results for exchange of inoculum between adjacent plots. The results of this model indicate, that the difference in rust infection between the cultivars may be due to a reduced growth of the epidemic in young plants of cultivars Cortina and Carina. In older plants, the ranking in susceptibility was reversed, causing a less pronounced difference in infection between the cultivars. The growth of leek rust epidemics during the early stage of the epidemic in isolated plots was satisfactorily described by an exponential model.     

Measurement of healthy and diseased haulm area for assessing late blight epidemics in potatoes

The advantages of assessing disease severity by visual grading and by measuring healthy and diseased plant area were compared in four mild to moderate late blight epidemics during spring and in two severe epidemics during autumn in Israel. Disease progress curves obtained through visual grading showed a continuous increase, but the area of lesions tended to fluctuate during the cropping season and often reached a maximum in plots in which the total amount of foliage was also largest. The healthy haulm area differed with disease intensity and undefined seasonal and cultural influences. The decrease in healthy haulm area was not related to expansion of the blighted area only, but also to the breaking of plants at stem lesions. This phenomenon was especially evident in the warm spring season and was not determined by visual grading of disease severity. Each kind of assessment revealed different features of the epidemics and suited different applications. Visual grading enabled the easiest comparison of epidemic patterns. Lesion areas reflected patterns of inoculum potential, while healthy haulm areas reflected the integrated influences of factors affecting the crop and disease and thus provided useful data for simulating epidemics and for estimating yield losses.