Scaling and spatial dynamics in plant-pathogen systems: from individuals to populations

Components of transmission for primary infection from soil-borne inoculum and secondary (plant to plant) infection are estimated from experiments involving single plants. The results from these individual-based experiments are used in a probabilistic spatial contact process (cellular automaton) to predict the progress of an epidemic. The model accounts for spatial correlations between infected and susceptible plants due to inhomogeneous mixing caused by restricted movement of the pathogen in soil. It also integrates nonlinearities in infection, including small stochastic differences in primary infection that become amplified by secondary infection. The model predicts both the mean and the variance of the infection dynamics of R. solani when compared with replicated epidemics in populations of plants grown in microcosms. The broader consequences of the combination of experimental and modelling approaches for scaling-up from individual to population behaviour are discussed. <br>     

Population dynamics of plant-parasite interactions: thresholds for invasion

Thresholds are derived for the invasion of plant populations by parasites. The theory is developed for a generic model that takes into account two features characteristic of plant-parasite interactions: a dual source of inoculum (infection from primary or externally introduced inoculum and secondary infection from contact between susceptible and infected host tissue) and a host response to infection load. Each of the threshold criteria is shown to be the sum of the individual components for primary and secondary infection. This indicates that if parasite invasion is not possible through primary or secondary infection alone, when the two modes of transmission are combined, the parasite may be able to invade. The invasion criteria demonstrate that there is a threshold population of susceptible hosts below which the parasite is unable to invade. If there are nonlinearities in the population dynamics (arising through either the transmission process or the host response), there are also threshold densities for the infected hosts and parasite populations below which invasion does not occur. The implications of the results for the control of plant disease are discussed.     

The role of initial inoculum on epidemic dynamics

Transient dynamics are important in many epidemics in agricultural and ecological systems that are prone to regular disturbance, cyclical and random perturbations. Here, using a simple host-pathogen model for a sessile host and a pathogen that can move by diffusion and advection, we use a range of mathematical techniques to examine the effect of initial spatial distribution of inoculum of the pathogen on the transient dynamics of the epidemic. We consider an isolated patch and a group of patches with different boundary conditions. We first determine bounds on the host population for the full model, then non-dimensionalizing the model allows us to obtain approximate solutions for the system. We identify two biologically intuitive groups of parameters to analyse transient behaviour using perturbation techniques. The first parameter group is a measure of the relative strength of initial primary to secondary infection. The second group is derived from the ratio of host removal rate (via infection) to pathogen removal rate (by decay and natural mortality) and measures the infectivity of initial inoculum on the system. By restricting the model to mimic primary infection only (in which all infections arise from initial inoculum), we obtain exact solutions and demonstrate how these depend on initial conditions, boundary conditions and model parameters. Finally, we suggest that the analyses on the balance of primary and secondary infection provide the epidemiologist with some simple rules to predict the transient behaviours.     

Potential of yeasts as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters

Among soil microorganisms, yeasts have received little attention as biocontrol agents of soil-borne fungal plant pathogens in comparison to bacterial, actinomycetes, and filamentous fungal antagonists. The mechanisms of action of potential antagonism by yeasts in relation to soil-borne fungal plant pathogens are expected to be similar to those involved with pathogens of aerial parts of the plant, including leaves and fruits. Several taxa of yeasts have been recorded as endophytes in plants, with a small proportion recorded to promote plant growth. The ability of certain taxa of yeasts to multiply rapidly, to produce antibiotics and cell wall-degrading enzymes, to induce resistance of host tissues, and to produce plant growth regulators indicates the potential to exploit them as biocontrol agents and plant growth promoters. More than ten genera of yeasts have been used to control postharvest diseases, especially of fruits. Suppression of classes of fungal pathogens of fruits and foliage that are similar to those associated with soil-borne fungal root pathogens, strongly suggests that yeasts also have potential for the biological control of diseases caused by soil-borne fungal plant pathogens, as is evident in reports of certain yeasts in suppressing some soil-borne fungal plant pathogens. This review explores the potential of soil yeasts to suppress a wider range of soil-borne fungal plant pathogens and to promote plant growth.     

Interplay between Parasitism and Host Ontogenic Resistance in the Epidemiology of the Soil-Borne Plant Pathogen Rhizoctonia solani

Spread of soil-borne fungal plant pathogens is mainly driven by the amount of resources the pathogen is able to capture and exploit should it behave either as a saprotroph or a parasite. Despite their importance in understanding the fungal spread in agricultural ecosystems, experimental data related to exploitation of infected host plants by the pathogen remain scarce. Using Rhizoctonia solani / Raphanus sativus as a model pathosystem, we have obtained evidence on the link between ontogenic resistance of a tuberizing host and (i) its susceptibility to the pathogen and (ii) after infection, the ability of the fungus to spread in soil. Based on a highly replicable experimental system, we first show that infection success strongly depends on the host phenological stage. The nature of the disease symptoms abruptly changes depending on whether infection occurred before or after host tuberization, switching from damping-off to necrosis respectively. Our investigations also demonstrate that fungal spread in soil still depends on the host phenological stage at the moment of infection. High, medium, or low spread occurred when infection was respectively before, during, or after the tuberization process. Implications for crop protection are discussed.     

Factors affecting host range in a generalist seed pathogen of semi-arid shrublands

Generalist pathogens can exhibit differential success on different hosts, resulting in complex host range patterns. Several factors operate to reduce realized host range relative to potential host range, particularly under field conditions. We explored factors influencing host range of the naturally occurring generalist ascomycete grass seed pathogen Pyrenophora semeniperda. We measured potential host range in laboratory experiments at high inoculum loads with 26 grass species, including the primary host Bromus tectorum, and developed models to predict susceptibility and tolerance based on host traits, including germination speed, seed hardness, seed size, and phylogenetic relations. We also examined pathogen and host density effects on infection and mortality. All species tested were at least somewhat susceptible to the pathogen at high inoculum loads, but both infection and mortality varied widely. Species more closely related to the original host (B. tectorum) were more susceptible to infection, whereas species with slower germination were less tolerant and therefore more likely to suffer mortality. Infection and mortality were sharply reduced as inoculum load was reduced. Intermediate loads had major negative impacts on dormant B. tectorum seeds but generally minimal effects on native species. In addition, field seed bank studies determined that P. semeniperda rarely exploits native grass species as hosts. This marked reduction in realized host range relative to potential host range indicates that laboratory host range studies are potentially a poor predictor of either the current or possible future realized host range for wildland plant pathogens.     

Virulence and community dynamics of fungal species with vertical and horizontal transmission on a plant with multiple infections

The virulence evolution of multiple infections of parasites from the same species has been modeled widely in evolution theory. However, experimental studies on this topic remain scarce, particularly regarding multiple infections by different parasite species. Here, we characterized the virulence and community dynamics of fungal pathogens on the invasive plant Ageratina adenophora to verify the predictions made by the model. We observed that A. adenophora was highly susceptible to diverse foliar pathogens with mixed vertical and horizontal transmission within leaf spots. The transmission mode mainly determined the pathogen community structure at the leaf spot level. Over time, the pathogen community within a leaf spot showed decreased Shannon diversity; moreover, the vertically transmitted pathogens exhibited decreased virulence to the host A. adenophora, but the horizontally transmitted pathogens exhibited increased virulence to the host. Our results demonstrate that the predictions of classical models for the virulence evolution of multiple infections are still valid in a complex realistic environment and highlight the impact of transmission mode on disease epidemics of foliar fungal pathogens. We also propose that seedborne fungi play an important role in structuring the foliar pathogen community from multiple infections within a leaf spot.     

Scaling from mycelial growth to infection dynamics: a reaction diffusion approach

Numerous models have been proposed for the dynamics of fungal growth, and also for the dynamics of infection. Few models, however, have combined the mechanistic interpretation of mycelial growth with epidemiological models for the transmission of infection. Many of the mechanistic models seek to include considerable biological detail, which necessarily leads to a proliferation of state variables and parameters. Including such models within an epidemiological framework makes interpretation of underpinning processes difficult. A simple reaction diffusion model for the growth and spread of fungal mycelium is introduced and analysed, scaling from the small-scale parameters for mycelial dynamics to the large-scale properties of the colony. By coupling the output to a parsimonious epidemiological model for the dynamics of primary infection, we analyse the sensitivity of the probability of successful infection of a host to the colony dynamics associated with local bulking-up, extension, growth and nutrient consumption by the mycelium. In particular we identify optimal trade-offs in bulking-up versus dispersal in controlling infection dynamics.     

An epidemiological framework for modelling fungicide dynamics and control

Defining appropriate policies for controlling the spread of fungal disease in agricultural landscapes requires appropriate theoretical models. Most existing models for the fungicidal control of plant diseases do not explicitly include the dynamics of the fungicide itself, nor do they consider the impact of infection occurring during the host growth phase. We introduce a modelling framework for fungicide application that allows us to consider how "explicit" modelling of fungicide dynamics affects the invasion and persistence of plant pathogens. Specifically, we show that "explicit" models exhibit bistability zones for values of the basic reproductive number ([Formula: see text]) less than one within which the invasion and persistence threshold depends on the initial infection levels. This is in contrast to classical models where invasion and persistence thresholds are solely dependent on [Formula: see text]. In addition if initial infection occurs during the growth phase then an additional "invasion zone" can exist for even smaller values of [Formula: see text]. Within this region the system will experience an epidemic that is not able to persist. We further show that ideal fungicides with high levels of effectiveness, low rates of application and low rates of decay lead to the existence of these bistability zones. The results are robust to the inclusion of demographic stochasticity.     

Secretome analysis of the phytopathogen Macrophomina phaseolina cultivated in liquid medium supplemented with and without soybean leaf infusion

Macrophomina phaseolina (Tassi) Goid. is a fungal pathogen that causes root and stem rot in several economically important crops. However, most of disease control strategies have shown limited effectiveness. Despite its impact on agriculture, molecular mechanisms involved in the interaction with host plant remains poorly understood. Nevertheless, it has been proven that fungal pathogens secrete a variety of proteins and metabolites to successfully infect their host plants. In this study, a proteomic analysis of proteins secreted by M. phaseolina in culture media supplemented with soybean leaf infusion was performed. A total of 250 proteins were identified with a predominance of hydrolytic enzymes. Plant cell wall degrading enzymes together peptidases were found, probably involved in the infection process. Predicted effector proteins were also found that could induce plant cell death or suppress plant immune response. Some of the putative effectors presented similarities to known fungal virulence factors. Expression analysis of ten selected protein-coding genes showed that these genes are induced during host tissue infection and suggested their participation in the infection process. The identification of secreted proteins of M. phaseolina could be used to improve the understanding of the biology and pathogenesis of this fungus. Although leaf infusion was able to induce changes at the proteome level, it is necessary to study the changes induced under conditions that mimic the natural infection process of the soil-borne pathogen M. phaseolina to identify virulence factors.     

The potential for rust infection to cause natural selection in apomictic Arabis holboellii (Brassicaceae)

Few studies have examined the potential for pathogens with complex life cycles to cause selection on their required alternate (=intermediate) hosts. Here we examine the effects of two fungal pathogens on an herbaceous mustard, Arabis holboellii. One pathogen species uses A. holboellii as a primary host, the other uses it as an alternate host. This plant-pathogen system is especially interesting because the host, A. holboellii, is apomictic; thus individuals reproduce exact copies of themselves. Despite this mode of reproduction, A. holboellii populations are surprisingly genetically diverse. Could frequency dependent selection by pathogens be maintaining clonal diversity? This study assesses the potential for selection by pathogens. In a controlled greehouse experiment we show that there is heritable variation in A. holboellii's resistance to the rust, Puccinia monoica, and that host fitness is severely reduced by P. monoica infection in both the greenhouse and under natural conditions. Field observations indicate that host clones are also differentially susceptible to the short-cycled rust, P. thlaspeos, and that host fitness is reduced by infection to this pathogen as well. Although the preconditions for pathogen-mediated selection are present, frequency-dependent selection by pathogens is unlikely to be important in structuring populations of Arabis holboellii because multiple host genotypes are susceptible to the same inoculum and the pathogen has a long generation time.     

The adaptive dynamics of the evolution of host resistance to indirectly transmitted microparasites

We use adaptive dynamics and pairwise invadability plots to examine the evolutionary dynamics of host resistance to microparasitic infection transmitted indirectly via free stages. We investigate trade-offs between pathogen transmission rate and intrinsic growth rate. Adaptive dynamics distinguishes various evolutionary outcomes associated with repellors, attractors or branching points. We find criteria corresponding to these and demonstrate that a major factor deciding the evolutionary outcome is whether trade-offs are acceleratingly or deceleratingly costly. We compare and contrast two models and show how the differences between them lead to different evolutionary outcomes.     

Dose-dependent infection rates of parasites produce the Allee effect in epidemiology

In many epidemiological models of microparasitic infections it is assumed that the infection process is governed by the mass-action principle, i.e. that the infection rate per host and per parasite is a constant. Furthermore, the parasite-induced host mortality (parasite virulence) and the reproduction rate of the parasite are often assumed to be independent of the infecting parasite dose. However, there is empirical evidence against those three assumptions: the infection rate per host is often found to be a sigmoidal rather than a linear function of the parasite dose to which it is exposed; and the lifespan of infected hosts as well as the reproduction rate of the parasite are often negatively correlated with the parasite dose. Here, we incorporate dose dependences into the standard modelling framework for microparasitic infections, and draw conclusions on the resulting dynamics. Our model displays an Allee effect that is characterized by an invasion threshold for the parasite. Furthermore, in contrast to standard epidemiological models a parasite strain needs to have a basic reproductive rate that is substantially greater than 1 to establish an infection. Thus, the conditions for successful invasion of the parasite are more restrictive than in mass-action infection models. The analysis further suggests that negative correlations of the parasite dose with host lifespan and the parasite reproduction rate helps the parasite to overcome the invasion constraints of the Allee-type dynamics.     

The Relationship between Host Lifespan and Pathogen Reservoir Potential: An Analysis in the System Arabidopsis thaliana-Cucumber mosaic virus

Identification of the determinants of pathogen reservoir potential is central to understand disease emergence. It has been proposed that host lifespan is one such determinant: short-lived hosts will invest less in costly defenses against pathogens, so that they will be more susceptible to infection, more competent as sources of infection and/or will sustain larger vector populations, thus being effective reservoirs for the infection of long-lived hosts. This hypothesis is sustained by analyses of different hosts of multihost pathogens, but not of different genotypes of the same host species. Here we examined this hypothesis by comparing two genotypes of the plant Arabidopsis thaliana that differ largely both in life-span and in tolerance to its natural pathogen Cucumber mosaic virus (CMV). Experiments with the aphid vector Myzus persicae showed that both genotypes were similarly competent as sources for virus transmission, but the short-lived genotype was more susceptible to infection and was able to sustain larger vector populations. To explore how differences in defense against CMV and its vector relate to reservoir potential, we developed a model that was run for a set of experimentally-determined parameters, and for a realistic range of host plant and vector population densities. Model simulations showed that the less efficient defenses of the short-lived genotype resulted in higher reservoir potential, which in heterogeneous host populations may be balanced by the longer infectious period of the long-lived genotype. This balance was modulated by the demography of both host and vector populations, and by the genetic composition of the host population. Thus, within-species genetic diversity for lifespan and defenses against pathogens will result in polymorphisms for pathogen reservoir potential, which will condition within-population infection dynamics. These results are relevant for a better understanding of host-pathogen co-evolution, and of the dynamics of pathogen emergence.     

内生真菌感染对宿主羊草抗病性的影响

以感染内生真菌的天然禾草羊草为实验材料,通过体外纯培养条件下的内生真菌、感染内生真菌的离体叶片和在体叶片对3种病原菌的抑菌实验,以探讨内生真菌对宿主植物羊草在抗病性方面的贡献。结果表明:体外纯培养条件下,分离自羊草的内生真菌Epichlobromicola对新月弯孢(Curvularia lunata)、根腐离蠕孢(Bipolaris sorokiniana)和枝孢霉(Cladosporium sp.)这3种病原菌都具有抑制作用,抑菌率分别达56.22%,46.93%和45.15%,且内生真菌培养滤液可以有效抑制这3种病原菌的孢子萌发,平均萌发率分别为30.4%,15.7%和16.4%;宿主植物叶片在离体条件下,内生真菌感染可以有效降低羊草叶片受C.lunata和C.sp.侵染后的病斑数或病斑长度,但对B.sorokiniana不起作用,甚至提高了叶片的病斑数及病斑长度,而离体叶片提取液对不同病原菌均有不同程度的抑制作用;在体条件下,内生真菌均可以通过降低叶片病斑数来增强羊草植株对这3种病原菌的抗性。由此看来,内生真菌E.bromicola对宿主植物羊草在抗病原菌侵染方面有一定的增益作用。     

The Relative Importance of Fungal Infection,Conspecific Density and Environmental Heterogeneity for Seedling Survival in a Dominant Tropical Tree

A gap remains in our understanding of how host‐specific fungal pathogens impact negative density dependence (NDD). Here, we investigated survival of Cinnamomum subavenium Miq. seedlings, the dominant canopy species in a seasonal tropical evergreen forest, Thailand. It is infected by a host‐specific fungus that is easily identifiable in the field. We quantified the effects of conspecific seedling and adult density on fungal infection and seedling survival over a wide range of environmental heterogeneity in elevation, understory vegetation and presence of forest gaps. Generalized linear mixed models (GLMMs) for seedling survival revealed that fungal infection significantly reduced survival and had the strongest effect on seedling survival as compared with conspecific density and environmental heterogeneity. Adult conspecific density was not, however, significantly correlated with the probability of infection, and conspecific seedling density was positively associated with increased infection only at high elevations. In contrast to infection, we found a significant positive correlation between conspecific seedling density and the probability of seedling survival. Consequently, our results demonstrate that fungal infection can have major impacts on seedling survival, but not in a manner consistent with local NDD effects on seedlings, as assumed in the Janzen–Connell hypothesis. Our study provides an example of how quantifying the interaction between environmental heterogeneity and a host‐specific plant‐pathogen can yield unexpected insights into the dynamics of seedling populations. The combined effects of host‐specific pathogens and environmental heterogeneity on survival of dominant seedling species may ultimately provide a chance for rarer species to recruit.