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1.
PLoS Comput Biol ; 19(11): e1011627, 2023 Nov.
Article in English | MEDLINE | ID: mdl-37983276

ABSTRACT

Within-host spread of pathogens is an important process for the study of plant-pathogen interactions. However, the development of plant-pathogen lesions remains practically difficult to characterize beyond the common traits such as lesion area. Here, we address this question by combining image-based phenotyping with mathematical modelling. We consider the spread of Peyronellaea pinodes on pea stipules that were monitored daily with visible imaging. We assume that pathogen propagation on host-tissues can be described by the Fisher-KPP model where lesion spread depends on both a logistic growth and an homogeneous diffusion. Model parameters are estimated using a variational data assimilation approach on sets of registered images. This modelling framework is used to compare the spread of an aggressive isolate on two pea cultivars with contrasted levels of partial resistance. We show that the expected slower spread on the most resistant cultivar is actually due to a significantly lower diffusion coefficient. This study shows that combining imaging with spatial mechanistic models can offer a mean to disentangle some processes involved in host-pathogen interactions and further development may allow a better identification of quantitative traits thereafter used in genetics and ecological studies.


Subject(s)
Host-Pathogen Interactions , Plant Diseases , Models, Biological , Plants
2.
Phytopathology ; 112(2): 414-421, 2022 Feb.
Article in English | MEDLINE | ID: mdl-34080915

ABSTRACT

Until recently, genotypes of Phytophthora infestans were regionally distributed in Europe, with populations in western Europe being dominated by clonal lineages and those in northern Europe being genetically diverse because of frequent sexual reproduction. However, since 2013 a new clonal lineage (EU_41_A2) has successfully established itself and expanded in the sexually recombining P. infestans populations of northern Europe. The objective of this study was to study phenotypic traits of the new clonal lineage of P. infestans, which may explain its successful establishment and expansion within sexually recombining populations. Fungicide sensitivity, aggressiveness, and virulence profiles of isolates of EU_41_A2 were analyzed and compared with those of the local sexual populations from Denmark, Norway, and Estonia. None of the phenotypic data obtained from the isolates collected from Denmark, Estonia, and Norway independently explained the invasive success of EU_41_A2 within sexual Nordic populations. Therefore, we hypothesize that the expansion of this new genotype could result from a combination of fitness traits and more favorable environmental conditions that have emerged in response to climate change.


Subject(s)
Phytophthora infestans , Solanum tuberosum , Genotype , Phenotype , Phytophthora infestans/genetics , Plant Diseases
3.
J Theor Biol ; 534: 110976, 2022 02 07.
Article in English | MEDLINE | ID: mdl-34883120

ABSTRACT

Using spatialised population measurements and related geographic habitat data, it is feasible nowadays to derive parsimonious spatially explicit population models and to carry on their parameter estimation. To achieve such goal, reaction-diffusion models are common in conservation biology and agricultural plant health where they are used, for example, for landscape planning or epidemiological surveillance. Unfortunately, if the mathematical methods and computational power are readily available, biological measurements are not. Despite the high throughput of some habitat related remote sensors, the experimental cost of biological measurements are one of the worst bottleneck against a widespread usage of reaction-diffusion models. Hence we will recall some classical methods for optimal experimental design that we deem useful to spatial ecologist. Using two case studies, one in landscape ecology and one in conservation biology, we will show how to construct a priori experimental design minimizing variance of parameter estimates, enabling optimal experimental setup under constraints.


Subject(s)
Ecosystem , Plants , Diffusion , Models, Biological , Population Dynamics
4.
Proc Biol Sci ; 286(1912): 20191244, 2019 10 09.
Article in English | MEDLINE | ID: mdl-31575367

ABSTRACT

Assessing life-history traits of parasites on resistant hosts is crucial in evolutionary ecology. In the particular case of sporulating pathogens with growing lesions, phenotyping is difficult because one needs to disentangle properly pathogen spread from sporulation. By considering Phytophthora infestans on potato, we use mathematical modelling to tackle this issue and refine the assessment of pathogen response to quantitative host resistance. We elaborate a parsimonious leaf-scale model by convolving a lesion growth model and a sporulation function, after a latency period. This model is fitted to data obtained on two isolates inoculated on three cultivars with contrasted resistance level. Our results confirm a significant host-pathogen interaction on the various estimated traits, and a reduction of both pathogen spread and spore production, induced by host resistance. Most interestingly, we highlight that quantitative resistance also changes the sporulation function, the mode of which is significantly time-lagged. This alteration of the infectious period distribution on resistant hosts may have strong impacts on the dynamics of parasite populations, and should be considered when assessing the durability of disease control tactics based on plant resistance management. This inter-disciplinary work also supports the relevance of mechanistic models for analysing phenotypic data of plant-pathogen interactions.


Subject(s)
Host-Pathogen Interactions , Life History Traits , Phytophthora infestans/physiology , Solanum tuberosum/microbiology , Solanum tuberosum/physiology , Models, Biological , Plant Diseases/microbiology
5.
Risk Anal ; 39(1): 54-70, 2019 01.
Article in English | MEDLINE | ID: mdl-29228505

ABSTRACT

We developed a simulation model for quantifying the spatio-temporal distribution of contaminants (e.g., xenobiotics) and assessing the risk of exposed populations at the landscape level. The model is a spatio-temporal exposure-hazard model based on (i) tools of stochastic geometry (marked polygon and point processes) for structuring the landscape and describing the exposed individuals, (ii) a dispersal kernel describing the dissemination of contaminants from polygon sources, and (iii) an (eco)toxicological equation describing the toxicokinetics and dynamics of contaminants in affected individuals. The model was implemented in the briskaR package (biological risk assessment with R) of the R software. This article presents the model background, the use of the package in an illustrative example, namely, the effect of genetically modified maize pollen on nontarget Lepidoptera, and typical comparisons of landscape configurations that can be carried out with our model (different configurations lead to different mortality rates in the treated example). In real case studies, parameters and parametric functions encountered in the model will have to be precisely specified to obtain realistic measures of risk and impact and accurate comparisons of landscape configurations. Our modeling framework could be applied to study other risks related to agriculture, for instance, pathogen spread in crops or livestock, and could be adapted to cope with other hazards such as toxic emissions from industrial areas having health effects on surrounding populations. Moreover, the R package has the potential to help risk managers in running quantitative risk assessments and testing management strategies.


Subject(s)
Ecology , Risk Assessment/methods , Xenobiotics/chemistry , Agriculture , Algorithms , Animals , Butterflies , Computer Simulation , Crops, Agricultural , Genetic Engineering , Humans , Livestock , Models, Biological , Organisms, Genetically Modified , Plant Diseases , Pollen , Proportional Hazards Models , Software , Toxicology , Zea mays/genetics
6.
Sci Total Environ ; 624: 470-479, 2018 May 15.
Article in English | MEDLINE | ID: mdl-29268219

ABSTRACT

The cultivation of Genetically Modified (GM) crops may have substantial impacts on populations of non-target organisms (NTOs) in agroecosystems. These impacts should be assessed at larger spatial scales than the cultivated field, and, as landscape-scale experiments are difficult, if not impossible, modelling approaches are needed to address landscape risk management. We present an original stochastic and spatially explicit modelling framework for assessing the risk at the landscape level. We use techniques from spatial statistics for simulating simplified landscapes made up of (aggregated or non-aggregated) GM fields, neutral fields and NTO's habitat areas. The dispersal of toxic pollen grains is obtained by convolving the emission of GM plants and validated dispersal kernel functions while the locations of exposed individuals are drawn from a point process. By taking into account the adherence of the ambient pollen on plants, the loss of pollen due to climatic events, and, an experimentally-validated mortality-dose function we predict risk maps and provide a distribution giving how the risk varies within exposed individuals in the landscape. Then, we consider the impact of the Bt maize on Inachis io in worst-case scenarii where exposed individuals are located in the vicinity of GM fields and pollen shedding overlaps with larval emergence. We perform a Global Sensitivity Analysis (GSA) to explore numerically how our input parameters influence the risk. Our results confirm the important effects of pollen emission and loss. Most interestingly they highlight that the optimal spatial distribution of GM fields that mitigates the risk depends on our knowledge of the habitats of NTOs, and finally, moderate the influence of the dispersal kernel function.

7.
PLoS One ; 11(9): e0163221, 2016.
Article in English | MEDLINE | ID: mdl-27668731

ABSTRACT

Reducing our reliance on pesticides is an essential step towards the sustainability of agricultural production. One approach involves the rational use of pesticides combined with innovative crop management. Most control strategies currently focus on the temporal aspect of epidemics, e.g. determining the optimal date for spraying, regardless of the spatial mechanics and ecology of disease spread. Designing innovative pest management strategies incorporating the spatial aspect of epidemics involves thorough knowledge on how disease control affects the life-history traits of the pathogen. In this study, using Rhizoctonia solani/Raphanus sativus as an example of a soil-borne pathosystem, we investigated the effects of a chemical control currently used by growers, Monceren® L, on key epidemiological components (saprotrophic spread and infectivity). We tested the potential "shield effect" of Monceren® L on pathogenic spread in a site-specific application context, i.e. the efficiency of this chemical to contain the spread of the fungus from an infected host when application is spatially localized, in our case, a strip placed between the infected host and a recipient bait. Our results showed that Monceren® L mainly inhibits the saprotrophic spread of the fungus in soil and may prevent the fungus from reaching its host plant. However, perhaps surprisingly we did not detect any significant effect of the fungicide on the pathogen infectivity. Finally, highly localized application of the fungicide-a narrow strip of soil (12.5 mm wide) sprayed with Monceren® L-significantly decreased local transmission of the pathogen, suggesting lowered risk of occurrence of invasive epidemics. Our results highlight that detailed knowledge on epidemiological processes could contribute to the design of innovative management strategies based on precision agriculture tools to improve the efficacy of disease control and reduce pesticide use.

8.
PLoS One ; 9(1): e86568, 2014.
Article in English | MEDLINE | ID: mdl-24466153

ABSTRACT

Knowledge of the incubation period of infectious diseases (time between host infection and expression of disease symptoms) is crucial to our epidemiological understanding and the design of appropriate prevention and control policies. Plant diseases cause substantial damage to agricultural and arboricultural systems, but there is still very little information about how the incubation period varies within host populations. In this paper, we focus on the incubation period of soilborne plant pathogens, which are difficult to detect as they spread and infect the hosts underground and above-ground symptoms occur considerably later. We conducted experiments on Rhizoctonia solani in sugar beet, as an example patho-system, and used modelling approaches to estimate the incubation period distribution and demonstrate the impact of differing estimations on our epidemiological understanding of plant diseases. We present measurements of the incubation period obtained in field conditions, fit alternative probability models to the data, and show that the incubation period distribution changes with host age. By simulating spatially-explicit epidemiological models with different incubation-period distributions, we study the conditions for a significant time lag between epidemics of cryptic infection and the associated epidemics of symptomatic disease. We examine the sensitivity of this lag to differing distributional assumptions about the incubation period (i.e. exponential versus Gamma). We demonstrate that accurate information about the incubation period distribution of a pathosystem can be critical in assessing the true scale of pathogen invasion behind early disease symptoms in the field; likewise, it can be central to model-based prediction of epidemic risk and evaluation of disease management strategies. Our results highlight that reliance on observation of disease symptoms can cause significant delay in detection of soil-borne pathogen epidemics and mislead practitioners and epidemiologists about the timing, extent, and viability of disease control measures for limiting economic loss.


Subject(s)
Epidemics , Host-Pathogen Interactions , Infectious Disease Incubation Period , Models, Theoretical , Plant Diseases , Algorithms
9.
PLoS One ; 8(5): e63003, 2013.
Article in English | MEDLINE | ID: mdl-23667560

ABSTRACT

Invasive soilborne plant pathogens cause substantial damage to crops and natural populations, but our understanding of how to prevent their epidemics or reduce their damage is limited. A key and experimentally-tested concept in the epidemiology of soilborne plant diseases is that of a threshold spacing between hosts below which epidemics (invasive spread) can occur. We extend this paradigm by examining how plant-root growth may alter the conditions for occurrence of soilborne pathogen epidemics in plant populations. We hypothesise that host-root growth can 1) increase the probability of pathogen transmission between neighbouring plants and, consequently, 2) decrease the threshold spacing for epidemics to occur. We predict that, in systems initially below their threshold conditions, root growth can trigger soilborne pathogen epidemics through a switch from non-invasive to invasive behaviour, while in systems above threshold conditions root growth can enhance epidemic development. As an example pathosystem, we studied the fungus Rhizoctonia solani on sugar beet in field experiments. To address hypothesis 1, we recorded infections within inoculum-donor and host-recipient pairs of plants with differing spacing. We translated these observations into the individual-level concept of pathozone, a host-centred form of dispersal kernel. To test hypothesis 2 and our prediction, we used the pathozone to parameterise a stochastic model of pathogen spread in a host population, contrasting scenarios of spread with and without host growth. Our results support our hypotheses and prediction. We suggest that practitioners of agriculture and arboriculture account for root system expansion in order to reduce the risk of soilborne-disease epidemics. We discuss changes in crop design, including increasing plant spacing and using crop mixtures, for boosting crop resilience to invasion and damage by soilborne pathogens. We speculate that the disease-induced root growth observed in some pathosystems could be a pathogen strategy to increase its population through host manipulation.


Subject(s)
Crops, Agricultural/microbiology , Host-Pathogen Interactions/physiology , Models, Biological , Plant Diseases/microbiology , Plant Roots/microbiology , Rhizoctonia/physiology , Soil Microbiology , Computer Simulation , Plant Diseases/prevention & control , Plant Roots/growth & development , Population Dynamics , Rhizoctonia/pathogenicity
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