14 research outputs found

    Evolution within a given virulence phenotype (pathotype) is driven by changes in aggressiveness: a case study of French wheat leaf rust populations

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    Plant pathogens are constantly evolving and adapting to their environment, including their host. Virulence alleles emerge, and then increase, and sometimes decrease in frequency within pathogen populations in response to the fluctuating selection pressures imposed by the deployment of resistance genes. In some cases, these strong selection pressures cannot fully explain the evolution observed in pathogen populations. A previous study on the French population of Puccinia triticina, the causal agent of wheat leaf rust, showed that two major pathotypes — groups of isolates with a particular combination of virulences — predominated but then declined over the 2005-2016 period. The relative dynamics and the domination of these two pathotypes — 166 317 0 and 106 314 0 —, relative to the other pathotypes present in the population at a low frequency although compatible, i.e. virulent on several varieties deployed, could not be explained solely by the frequency of Lr genes in the landscape. Within these two pathotypes, we identified two main genotypes that emerged in succession. We assessed three components of aggressiveness — infection efficiency, latency period and sporulation capacity — for 44 isolates representative of the four P. triticina pathotype-genotype combinations. We showed, for both pathotypes, that the more recent genotypes were more aggressive than the older ones. Our findings were highly consistent for the various components of aggressiveness for pathotype 166 317 0 grown on Michigan Amber — a ‘naive’ cultivar never grown in the landscape — or on Apache — a ‘neutral’ cultivar, which does not affect the pathotype frequency in the landscape and therefore was postulated to have no or minor selection effect on the population composition. For pathotype 106 314 0, the most recent genotype had a shorter latency period on several of the cultivars most frequently grown in the landscape, but not on ‘neutral’ and ‘naive’ cultivars. We conclude that the quantitative components of aggressiveness can be significant drivers of evolution in pathogen populations. A gain in aggressiveness stopped the decline in frequency of a pathotype, and subsequently allowed an increase in frequency of this pathotype in the pathogen population, providing evidence that adaptation to a changing varietal landscape not only affects virulence but can also lead to changes in aggressiveness

    Diversity of thermal aptitude of Middle Eastern and Mediterranean Puccinia striiformis f. sp. tritici isolates from different altitude zones

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    The worldwide spread of wheat yellow rust lineage PstS1/S2 adapted to higher temperatures prompted us to investigate how diverse temperature responses of this lineage are in the Middle East, where diversity was previously observed within this lineage for pathotypes and genotypes. Here we highlight the diversity of response to temperature within a PstS1/S2 population. Twenty-six isolates from eight countries and different altitudes, which were tested under four combinations of cold and warm incubation and postincubation temperature conditions, showed diversity for infection efficiency (IE) and latency period (LP). IE of the various isolates ranged from 5.8% to 13.7% under cold (5°C) and 0.04% to 1% under warm (20°C) incubation temperatures. LP varied from 10.2 days under warm to 4.43 days under cold incubation. LP of isolates from the same country could differ by 2 days. Significant differences in thermal aptitudes of the isolates were observed between and within countries. IE and LP diversity was not related to altitude origin of the isolates on the whole; however, a trade-off between IE and LP was observed for isolates from low altitude (<400 m) under a warm regime. We showed diversity for thermal aptitude for IE and LP of isolates belonging to the same PstS1/S2 lineage. Understanding Pst temperature aptitude among geographically distant isolates of the same clonal lineage may help to identify the geographic range of pathogens and also to improve forecast models or breeding programmes

    "IntĂ©rĂȘt de la diversitĂ© spĂ©cifique et variĂ©tale Ă  l’échelle de la parcelle agricole pour limiter la progression d’une maladie : la septoriose du blĂ©"

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    Prix (2016) de la fondation Xavier Bernard de l’AcadĂ©mie d’agriculture de Franceil s'agit d'un type de produit dont les mĂ©tadonnĂ©es ne correspondent pas aux mĂ©tadonnĂ©es attendues dans les autres types de produit : DISSERTATION"IntĂ©rĂȘt de la diversitĂ© spĂ©cifique et variĂ©tale Ă  l’échelle de la parcelle agricole pour limiter la progression d’une maladie : la septoriose du blĂ©

    L’hĂ©tĂ©rogĂ©nĂ©itĂ© environnementale, un moteur de l’adaptation Ă  la tempĂ©rature des populations d’agents phytopathogĂšnes foliaires ?

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    Les facteurs environnementaux, au premier rang desquels la tempĂ©rature, ont un impact sur la biologie des micro-organismes foliaires. Ils peuvent aussi modifier significativement leurs dynamiques populationnelles, voire leurs trajectoires Ă©volutives. Classiquement, les modĂšles Ă©pidĂ©miologiques, utilisĂ©s pour mieux gĂ©rer les maladies des plantes, intĂšgrent l’influence des conditions mĂ©tĂ©orologiques. Ils s’intĂ©ressent surtout Ă  des rĂ©ponses et des effets moyennĂ©s, ne tenant compte ni des variations des rĂ©ponses individuelles, ni de l’hĂ©tĂ©rogĂ©nĂ©itĂ© des changements environnementaux aux Ă©chelles rĂ©ellement perçues par les agents pathogĂšnes. Ces deux niveaux de simplification sont acceptables lorsque les Ă©tats individuels et les variables continues qui leur sont associĂ©es, peu diversifiĂ©s, sont reprĂ©sentatifs de ceux de l'ensemble de la population. Il en va diffĂ©remment lorsque les populations prĂ©sentent des niveaux substantiels de variation individuelle susceptibles d’influencer leur capacitĂ© Ă  s’adapter Ă  leur environnement, et, par voie de consĂ©quence, la dynamique des Ă©pidĂ©mies sous un climat fluctuant ou changeant. Pour mettre en Ă©vidence les consĂ©quences de ces hypothĂšses rĂ©ductrices, j’ai Ă©tudiĂ© comment la variation individuelle et l'hĂ©tĂ©rogĂ©nĂ©itĂ© environnementale affectent simultanĂ©ment la fitness, la composition phĂ©notypique et la rĂ©silience des populations d'un agent pathogĂšne foliaire (Zymoseptoria tritici) dans des couverts de blĂ©. Trois Ă©tapes clĂ©s ont structurĂ© l’exploration de ce cas d’étude. Tout d’abord, un protocole in vitro de phĂ©notypage haut dĂ©bit a Ă©tĂ© spĂ©cifiquement dĂ©veloppĂ©, validĂ© et utilisĂ© pour caractĂ©riser la diversitĂ© des rĂ©ponses Ă  la tempĂ©rature de populations de Z. tritici Ă©chantillonnĂ©es Ă  des Ă©chelles climatiques contrastĂ©es (variation spatiale et saisonniĂšre) ainsi que leurs patrons d’adaptation. Les variations environnementales spatio-temporelles rencontrĂ©es dans les couverts de blĂ©, considĂ©rĂ©es comme exerçant des pressions sĂ©lectives diffĂ©rentielles sur ces sensibilitĂ©s thermiques individuelles, ont ensuite Ă©tĂ© examinĂ©es. Enfin, la façon dont la sĂ©lection de « thermotypes » (groupes fonctionnels rassemblant des individus prĂ©sentant une mĂȘme sensibilitĂ© thermique) dĂ©termine la dynamique adaptative des populations en rĂ©ponse Ă  l'hĂ©tĂ©rogĂ©nĂ©itĂ© environnementale a Ă©tĂ© Ă©tudiĂ©e. Pour cela, des approches expĂ©rimentales (in vitro, in planta et in natura) et de modĂ©lisation (in silico) ont Ă©tĂ© couplĂ©es. Elles ont notamment portĂ© sur plusieurs gĂ©nĂ©rations de populations placĂ©es dans des environnements sĂ©lectifs de plus en plus complexes. Ces travaux ont montrĂ© que le fait de nĂ©gliger l'amplitude rĂ©elle de la variation phĂ©notypique inter-individuelle d'une population microbienne et l'hĂ©tĂ©rogĂ©nĂ©itĂ© des pressions de sĂ©lection, s’exerçant des Ă©chelles phyllo- Ă  mĂ©soclimatiques, conduit Ă  sous-estimer la rĂ©silience de cette population, et donc son potentiel adaptatif. Les rĂ©sultats de cette thĂšse, Ă  l’interface entre Ă©pidĂ©miologie, micromĂ©tĂ©orologie et Ă©cologie, amĂ©liorent notre comprĂ©hension d’une part, de l'importance de la variation individuelle dans la dynamique adaptative des populations et, d’autre part, de la maniĂšre dont l'hĂ©tĂ©rogĂ©nĂ©itĂ© environnementale permet de maintenir des populations globalement trĂšs diverses. Elle permet finalement d’expliquer l’existence de patrons d’adaptation, Ă  la fois Ă  des Ă©chelles locales et Ă  des Ă©chelles trĂšs larges, par des dynamiques adaptatives «à deux vitesses».Environmental drivers, most notably temperature, affect the biology of phyllosphere microorganisms but also induce changes in their population dynamics, even in their evolutionary trajectories. The impact of climate on foliar plant disease epidemics is usually considered in forecasting models to inform management strategies. Such models focus on averages of environmental drivers but disregard both individual variation within populations and the scale and extent of biologically relevant environmental changes. These simplifications are glossing over substantial levels of individual variation that may have important consequences on the capacity of a population to adapt to environmental changes, and thus on the dynamics of epidemics in a fluctuating or changing climate. To examine the range of validity and consequences of these simplifying assumptions, I investigated how individual variation and environmental heterogeneity jointly affect fitness, phenotypic composition and resilience of populations of a foliar pathogen (Zymoseptoria tritici) inhabiting wheat canopies. Three complementary ways of exploration were adopted in this case study. First, an in vitro high-throughput phenotyping framework was developed, validated, and used to characterise the diversity in patterns of thermal responses existing across Z. tritici populations that were sampled over contrasted scales (spatial and seasonal variation of temperature). Second, the spatio-temporal thermal variations encountered in a wheat canopy, considered as a habitat exerting fluctuating selective pressures on these differential thermal sensitivities of individuals, were investigated in depth. Third, the way selection of “thermotypes” (functional groups of individuals displaying a similar thermal sensitivity) occurs and drives dynamics of Z. tritici populations was examined. To this end, both empirical (in vitro, in planta and in natura) and theoretical (in silico) competition experiments were conducted under increasingly complex selective environments. This research work demonstrates that glossing over the natural extent of individual phenotypic diversity in a phyllosphere microbial population and over the heterogeneity of selective pressures – from phyllo- to mesoclimate – leads to underestimate the resilience of this population, and thus its adaptive potential to environmental variations. In doing so, the results of this thesis, at the interface between epidemiology, micrometeorology, and ecology, improve our understanding of how important is individual variation to population dynamics and how environmental heterogeneity allows to maintain population diversity. Finally, this thesis provides insight into how large-scale patterns and local population processes are interlinked and display a “two-tier” adaptive dynamics

    Environmental heterogeneity, a driver of adaptation to temperature in foliar plant pathogen populations?

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    Environmental drivers, most notably temperature, affect the biology of phyllosphere microorganisms but also induce changes in their population dynamics, even in their evolutionary trajectories. The impact of climate on foliar plant disease epidemics is usually considered in forecasting models to inform management strategies. Such models focus on averages of environmental drivers but disregard both individual variation within populations and the scale and extent of biologically relevant environmental changes. These simplifications are glossing over substantial levels of individual variation that may have important consequences on the capacity of a population to adapt to environmental changes, and thus on the dynamics of epidemics in a fluctuating or changing climate. To examine the range of validity and consequences of these simplifying assumptions, I investigated how individual variation and environmental heterogeneity jointly affect fitness, phenotypic composition and resilience of populations of a foliar pathogen (Zymoseptoria tritici) inhabiting wheat canopies. Three complementary ways of exploration were adopted in this case study. First, an in vitro high-throughput phenotyping framework was developed, validated, and used to characterise the diversity in patterns of thermal responses existing across Z. tritici populations that were sampled over contrasted scales (spatial and seasonal variation of temperature). Second, the spatio-temporal thermal variations encountered in a wheat canopy, considered as a habitat exerting fluctuating selective pressures on these differential thermal sensitivities of individuals, were investigated in depth. Third, the way selection of “thermotypes” (functional groups of individuals displaying a similar thermal sensitivity) occurs and drives dynamics of Z. tritici populations was examined. To this end, both empirical (in vitro, in planta and in natura) and theoretical (in silico) competition experiments were conducted under increasingly complex selective environments. This research work demonstrates that glossing over the natural extent of individual phenotypic diversity in a phyllosphere microbial population and over the heterogeneity of selective pressures – from phyllo- to mesoclimate – leads to underestimate the resilience of this population, and thus its adaptive potential to environmental variations. In doing so, the results of this thesis, at the interface between epidemiology, micrometeorology, and ecology, improve our understanding of how important is individual variation to population dynamics and how environmental heterogeneity allows to maintain population diversity. Finally, this thesis provides insight into how large-scale patterns and local population processes are interlinked and display a “two-tier” adaptive dynamics.Les facteurs environnementaux, au premier rang desquels la tempĂ©rature, ont un impact sur la biologie des micro-organismes foliaires. Ils peuvent aussi modifier significativement leurs dynamiques populationnelles, voire leurs trajectoires Ă©volutives. Classiquement, les modĂšles Ă©pidĂ©miologiques, utilisĂ©s pour mieux gĂ©rer les maladies des plantes, intĂšgrent l’influence des conditions mĂ©tĂ©orologiques. Ils s’intĂ©ressent surtout Ă  des rĂ©ponses et des effets moyennĂ©s, ne tenant compte ni des variations des rĂ©ponses individuelles, ni de l’hĂ©tĂ©rogĂ©nĂ©itĂ© des changements environnementaux aux Ă©chelles rĂ©ellement perçues par les agents pathogĂšnes. Ces deux niveaux de simplification sont acceptables lorsque les Ă©tats individuels et les variables continues qui leur sont associĂ©es, peu diversifiĂ©s, sont reprĂ©sentatifs de ceux de l'ensemble de la population. Il en va diffĂ©remment lorsque les populations prĂ©sentent des niveaux substantiels de variation individuelle susceptibles d’influencer leur capacitĂ© Ă  s’adapter Ă  leur environnement, et, par voie de consĂ©quence, la dynamique des Ă©pidĂ©mies sous un climat fluctuant ou changeant. Pour mettre en Ă©vidence les consĂ©quences de ces hypothĂšses rĂ©ductrices, j’ai Ă©tudiĂ© comment la variation individuelle et l'hĂ©tĂ©rogĂ©nĂ©itĂ© environnementale affectent simultanĂ©ment la fitness, la composition phĂ©notypique et la rĂ©silience des populations d'un agent pathogĂšne foliaire (Zymoseptoria tritici) dans des couverts de blĂ©. Trois Ă©tapes clĂ©s ont structurĂ© l’exploration de ce cas d’étude. Tout d’abord, un protocole in vitro de phĂ©notypage haut dĂ©bit a Ă©tĂ© spĂ©cifiquement dĂ©veloppĂ©, validĂ© et utilisĂ© pour caractĂ©riser la diversitĂ© des rĂ©ponses Ă  la tempĂ©rature de populations de Z. tritici Ă©chantillonnĂ©es Ă  des Ă©chelles climatiques contrastĂ©es (variation spatiale et saisonniĂšre) ainsi que leurs patrons d’adaptation. Les variations environnementales spatio-temporelles rencontrĂ©es dans les couverts de blĂ©, considĂ©rĂ©es comme exerçant des pressions sĂ©lectives diffĂ©rentielles sur ces sensibilitĂ©s thermiques individuelles, ont ensuite Ă©tĂ© examinĂ©es. Enfin, la façon dont la sĂ©lection de « thermotypes » (groupes fonctionnels rassemblant des individus prĂ©sentant une mĂȘme sensibilitĂ© thermique) dĂ©termine la dynamique adaptative des populations en rĂ©ponse Ă  l'hĂ©tĂ©rogĂ©nĂ©itĂ© environnementale a Ă©tĂ© Ă©tudiĂ©e. Pour cela, des approches expĂ©rimentales (in vitro, in planta et in natura) et de modĂ©lisation (in silico) ont Ă©tĂ© couplĂ©es. Elles ont notamment portĂ© sur plusieurs gĂ©nĂ©rations de populations placĂ©es dans des environnements sĂ©lectifs de plus en plus complexes. Ces travaux ont montrĂ© que le fait de nĂ©gliger l'amplitude rĂ©elle de la variation phĂ©notypique inter-individuelle d'une population microbienne et l'hĂ©tĂ©rogĂ©nĂ©itĂ© des pressions de sĂ©lection, s’exerçant des Ă©chelles phyllo- Ă  mĂ©soclimatiques, conduit Ă  sous-estimer la rĂ©silience de cette population, et donc son potentiel adaptatif. Les rĂ©sultats de cette thĂšse, Ă  l’interface entre Ă©pidĂ©miologie, micromĂ©tĂ©orologie et Ă©cologie, amĂ©liorent notre comprĂ©hension d’une part, de l'importance de la variation individuelle dans la dynamique adaptative des populations et, d’autre part, de la maniĂšre dont l'hĂ©tĂ©rogĂ©nĂ©itĂ© environnementale permet de maintenir des populations globalement trĂšs diverses. Elle permet finalement d’expliquer l’existence de patrons d’adaptation, Ă  la fois Ă  des Ă©chelles locales et Ă  des Ă©chelles trĂšs larges, par des dynamiques adaptatives «à deux vitesses»

    Diversifier les paysages cultivés : état des connaissances et perspectives de recherche

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    International audienceDiversifier les paysages cultivés : état des connaissances et perspectives de recherche Chapitre tiré de l'ouvrage « L'immunité des plantes » Edition Quae, 2021

    Diversifier les paysages cultivés : état des connaissances et perspectives de recherche

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    International audienceDiversifier les paysages cultivĂ©s : Ă©tat des connaissances et perspectives de recherche Chapitre 19tirĂ© de l'ouvrage « L'immunitĂ© des plantes »PrĂ©sentation de l'ouvrageLes plantes disposent d’une immunitĂ© naturelle qui leur permet de rĂ©sister aux maladies et aux agressions parasitaires dans leur environnement. L’invention puis le dĂ©veloppement de l’agriculture ont cependant crĂ©Ă© des milieux trĂšs favorables Ă  l’émergence de nouvelles maladies et au dĂ©veloppement des Ă©pidĂ©mies. Cette vulnĂ©rabilitĂ© sanitaire s’est ensuite accentuĂ©e avec l’intensification agricole, Ă  partir des annĂ©es 1950, de sorte que le recours gĂ©nĂ©ralisĂ© aux pesticides de synthĂšse est devenu un pilier essentiel de la production. Ce modĂšle est dĂ©sormais remis en cause et le dĂ©veloppement d’une protection agroĂ©cologique des cultures devient une nĂ©cessitĂ©.Comprendre comment fonctionne l’immunitĂ© des plantes et dĂ©chiffrer leur arsenal de dĂ©fense face aux agressions parasitaires est essentiel pour produire des variĂ©tĂ©s rĂ©sistantes et rĂ©duire la dĂ©pendance de l’agriculture Ă  la protection chimique. Mais il faut compter avec la formidable capacitĂ© d’adaptation des populations pathogĂšnes, qui conduit les chercheurs Ă  imaginer des stratĂ©gies complexes pour maintenir efficace la rĂ©sistance des variĂ©tĂ©s cultivĂ©es. Les gĂšnes qui confĂšrent la rĂ©sistance aux plantes commencent Ă  ĂȘtre perçus comme un bien commun Ă  prĂ©server absolument.Cet ouvrage explicite les concepts fondamentaux et s’appuie sur des Ă©tudes de cas pour rĂ©aliser une synthĂšse trĂšs complĂšte des travaux en biologie, en modĂ©lisation et en sciences sociales sur ce qu’est l’immunitĂ© vĂ©gĂ©tale et sur la maniĂšre dont elle pourrait concourir Ă  une agriculture respectueuse de l’environnement

    Slipping through the cracks: Challenges and prospects for investigating fungal plant disease complexes

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    International audiencePlant pathogens frequently do not operate alone when causing diseases. Since the infection process is affected by the interaction between members of the parasite community, this question asks about the efficiency of disease control strategies which are usually tailored to manage only one microbial pathogen at a time. Fungi and oomycetes are among plant disease's most prevalent and damaging causal agents. With the increasing ability to distinguish individual species, thanks to new high-throughput molecular tools, numerous diseases once attributed to a single species are now recognized as being caused by complexes of fungal phytopathogens. How should we approach the study of these complexes? What tools and methodologies are needed to characterize them and decipher their functional interactions? How can we understand and master the drivers of these coinfections and their dynamics under field conditions? Here, we review the current literature on fungal disease complexes to define their commonalities and address some of the current challenges regarding the identification of preferential associations among fungal species indicative of a disease complex and its community dynamics and regulation. This review highlights that fungal species complexes are highly dynamic at geographic and temporal scales and that human actions contributed to the dissemination of new members of species complexes worldwide and to disequilibrium within species complexes, often resulting in more damaging diseases. This review also points to the generally insufficient (or lacking) knowledge of the diversity, dynamics, and functioning of fungal disease complexes, and the risks linked with inappropriate management strategies focusing on only one dominant member of the complex

    Hunting for sources of durable resistance in crop cultivar evaluation data: The case of wheat yellow rust in France

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    International audienceAbstract Cultivar resistance is a major asset for the management of crop diseases and can play an important role in agroecological transition. However, the wide deployment of a reduced number of resistance genes can lead to a rapid adaptation of pathogen populations and to a loss of resistance efficiency. The objective of this study was to characterize and discuss different trajectories of adult plant ratings for resistance to yellow rust in French wheat cultivars between 1963 and 2018. Among 719 cultivars assessed for at least 2 years, 590 cultivars showed no variation in their resistance scores, despite a mean of 4.3 years and up to 33 years of assessment. A set of descriptive variables was computed in order to compare the evolution of resistance score of 129 cultivars that experienced resistance variation. We applied a principal component analysis and a hierarchical clustering on principal components to this subdataset to constitute clusters corresponding to different cultivar profiles. Clusters C1 and C2 had small resistance variations (1–2 points on a 1–9 scale); Cluster C3 had long assessment durations and several small drops in resistance score and could be associated with quantitative resistance erosion; Cluster C4 included major drops in resistance score (4–5 points), often associated with known breakdowns of major resistance genes. Cases of limited drops in resistance score as a known resistance gene was broken down suggest the presence of efficient adult plant resistance. We discuss the use of information extracted from this dataset and methods to further explore sources of resistance to yellow rust present in French cultivars
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