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Virus epidemics, plant-controlled population bottlenecks and the durability of plant resistance.

ABSTRACT: Plant qualitative resistances to viruses are natural exhaustible resources that can be impaired by the emergence of resistance-breaking (RB) virus variants. Mathematical modelling can help determine optimal strategies for resistance durability by a rational deployment of resistance in agroecosystems. Here, we propose an innovative approach, built up from our previous empirical studies, based on plant cultivars combining qualitative resistance with quantitative resistance narrowing population bottlenecks exerted on viruses during host-to-host transmission and/or within-host infection. Narrow bottlenecks are expected to slow down virus adaptation to plant qualitative resistance. To study the effect of bottleneck size on yield, we developed a stochastic epidemic model with mixtures of susceptible and resistant plants, relying on continuous-time Markov chain processes. Overall, narrow bottlenecks are beneficial when the fitness cost of RB virus variants in susceptible plants is intermediate. In such cases, they could provide up to 95 additional percentage points of yield compared with deploying a qualitative resistance alone. As we have shown in previous works that virus population bottlenecks are at least partly heritable plant traits, our results suggest that breeding and deploying plant varieties exposing virus populations to narrowed bottlenecks will increase yield and delay the emergence of RB variants. This article is part of the theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: approaches and important themes'. This issue is linked with the subsequent theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: epidemic forecasting and control'.

SUBMITTER: Rousseau E

PROVIDER: S-EPMC6553610 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Virus epidemics, plant-controlled population bottlenecks and the durability of plant resistance.

Rousseau Elsa E Bonneault Mélanie M Fabre Frédéric F Moury Benoît B Mailleret Ludovic L Grognard Frédéric F

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20190601 1775

Plant qualitative resistances to viruses are natural exhaustible resources that can be impaired by the emergence of resistance-breaking (RB) virus variants. Mathematical modelling can help determine optimal strategies for resistance durability by a rational deployment of resistance in agroecosystems. Here, we propose an innovative approach, built up from our previous empirical studies, based on plant cultivars combining qualitative resistance with quantitative resistance narrowing population bot ...[more]

PMID: 31056046

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Project description:Rice black-streaked dwarf virus (RBSDV) (species Rice black-streaked dwarf virus, genus Fijivirus, family Reoviridae) is the causal agent of rice black-streaked dwarf and maize rough dwarf diseases, which occur in intermittent epidemics in East Asian countries and are responsible for considerable yield losses. Intermittency of epidemics make accurate forecasting and designing of effective management strategies difficult. However, recent insights into host-virus-vector insect interactions are now informing forecasting and disease control measures. Resistance genes are also being identified and mapped.Symptomatology and host rangeRBSDV induces extreme stunting, darkened, and stiff leaves of crops and weeds only in the family Poaceae, including Oryza sativa, Zea mays, and Triticum aestivum. Infected plants produce totally or partially deformed panicles and remain alive through harvest.Genome and gene functionThe nonenveloped virus particles comprise a double-layered capsid, 50-nm core with genomic double-stranded RNA (dsRNA), and six proteins. The genome of RBSDV contains 10 segments of dsRNA, named S1 to S10 in decreasing order of molecular weight. Segments 1, 2, 3, 4, 6, 8, and 10 encode the RNA-dependent RNA polymerase (RdRp), the major core structural protein, a protein with guanylyltransferase activity, an outer-shell B-spike protein, viral RNA-silencing suppressor, the major capsid protein, and the outer capsid protein, respectively. Each of the segments 5, 7, and 9 encodes two proteins: P5-1, a component of viroplasms; P5-2 of unknown function; nonstructural protein P7-1, involved in forming the structural matrix of tubular structures in infected tissues; P7-2 of unknown function; P9-1, the main component of viroplasms in infected cells and involved in viral replication; and P9-2 of unknown function.Transmission and epidemiologyRBSDV is transmitted by Laodelphax striatellus in a persistent propagative manner. The vector insect is the only means of virus spread in nature, so its migration and transmission efficiency are obligatory for disease epidemics to develop. Susceptible varieties are widely planted, but efficient transmission by vectors is the primary reason for the epidemics. Cultivation system, pesticide overuse, and climatic conditions also contribute to epidemics by affecting the development of the vector insects and their population dynamics.Disease managementIn the absence of resistant varieties, integrated disease management aims at disrupting the cycle of virus transmission by the insect vector. Inheritance studies have indicated that resistance is mostly governed by quantitative trait loci or multiple genes. Genetic engineering through RNA-interference and gene-editing strategies are potential approaches for disease control.

Project description:Genetically-controlled plant resistance can reduce the damage caused by pathogens. However, pathogens have the ability to evolve and overcome such resistance. This often occurs quickly after resistance is deployed, resulting in significant crop losses and a continuing need to develop new resistant cultivars. To tackle this issue, several strategies have been proposed to constrain the evolution of pathogen populations and thus increase genetic resistance durability. These strategies mainly rely on varying different combinations of resistance sources across time (crop rotations) and space. The spatial scale of deployment can vary from multiple resistance sources occurring in a single cultivar (pyramiding), in different cultivars within the same field (cultivar mixtures) or in different fields (mosaics). However, experimental comparison of the efficiency (i.e. ability to reduce disease impact) and durability (i.e. ability to limit pathogen evolution and delay resistance breakdown) of landscape-scale deployment strategies presents major logistical challenges. Therefore, we developed a spatially explicit stochastic model able to assess the epidemiological and evolutionary outcomes of the four major deployment options described above, including both qualitative resistance (i.e. major genes) and quantitative resistance traits against several components of pathogen aggressiveness: infection rate, latent period duration, propagule production rate, and infectious period duration. This model, implemented in the R package landsepi, provides a new and useful tool to assess the performance of a wide range of deployment options, and helps investigate the effect of landscape, epidemiological and evolutionary parameters. This article describes the model and its parameterisation for rust diseases of cereal crops, caused by fungi of the genus Puccinia. To illustrate the model, we use it to assess the epidemiological and evolutionary potential of the combination of a major gene and different traits of quantitative resistance. The comparison of the four major deployment strategies described above will be the objective of future studies.

Project description:Background: Pathogens are often assumed to evolve towards reduced virulence, but counterexamples abound. Faced with a new pathogen, such as SARS-CoV-2, it is crucial to be able to forecast the case fatality rate (CFR) and the overall disease burden. Considerable effort has been invested towards developing a mathematical framework for predicting virulence evolution. Although many approaches accurately recapitulate complex outcomes, most rely on an assumed trade-off between CFR and infection rate. It is often impractical to empirically validate this constraint for human pathogens. Methods: A compartment model with parameters tuning the degree to which symptomatic individuals are isolated and the duration of immunity is constructed and evaluated at both short timescales and at equilibrium. Results: We reveal kinetic constraints whereby variation of multiple parameters in concert leads to decreased CFR and increased pathogen fitness, whereas independent variation of the parameters decreases pathogen fitness. Smallpox, SARS-CoV-2, and influenza are analyzed as diverse representatives of human respiratory viruses. We show that highly virulent viruses, such as smallpox, are often constrained by the host behavior, whereas moderately virulent viruses, such as SARS-CoV-2, appear to be typically constrained by the relationship between the duration of immunity and CFR. Conclusions: Evolution of human respiratory epidemics appears to be often kinetically constrained and a reduction in CFR should not be assumed. These results agree with previous work demonstrating an increase in virulence for smallpox and further predict that SARS-CoV-2 is likely to continue presenting a substantial disease burden. Herd immunity against SARS-CoV-2 and viruses with similar life history traits might be unachievable without vaccination. However, partial isolation of symptomatic individuals can have a major effect on the epidemic dynamics not only by reducing the number of fatalities in the short term but also by changing the evolutionary trajectory of moderate CFR viruses towards reduced CFR.

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Virus epidemics, plant-controlled population bottlenecks and the durability of plant resistance.

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Virus epidemics, plant-controlled population bottlenecks and the durability of plant resistance.

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