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Emergence and populations genomics of the highly invasive chestnut blight pathogen
Auteur(s)
Neuchâtel
Date Issued
2021
Subjects
Abstract
Les agents pathogènes envahissants constituent une menace pour les forêts et les agroécosystèmes, ainsi que pour la santé animale et humaine. L'identification des déterminants génomiques de l'évolution des agents pathogènes, ainsi que l’analyse de la structure génétique des populations d'agents pathogènes envahissants fournissent des informations fondamentales sur les raisons pour lesquelles des espèces peuvent devenir des agents pathogènes envahissants. Dans ce projet de doctorat, j'ai étudié l'émergence et la génomique des populations de la maladie du chancre de l’écorce du châtaignier qui est provoqué par le champignon envahissant <i>Cryphonectria parasitica</i>, en utilisant des approches de génomique comparative et de génomique des populations. <i>C. parasitica</i> est récemment apparu comme un pathogène envahissant de l'écorce sur des espèces de <i>Castanea</i> non asiatiques en Amérique du Nord et en Europe. Dans le premier chapitre, j'ai étudié les déterminants génomiques des transitions du mode de vie dans le genre <i>Cryphonectria</i>, en comparant le génome de <i>C. parasitica</i> et de ses espèces sœurs. L'étude a révélé une diminution frappante du nombre de gènes associés au métabolisme des glucides chez le pathogène envahissant <i>C. parasitica</i>, qui pourrait avoir favorisé sa pathogénicité sur les espèces de <i>Castanea</i>. Le deuxième chapitre explore l'émergence et la diversification d'une lignée de chancre du châtaignier très envahissante dans le sud-est de l'Europe. En analysant la diversité du génome d'un large ensemble d'isolats de <i>C. parasitica</i> d'origine principalement européenne, l'étude a montré qu'une lignée clonale envahissante du pathogène peut émerger à partir d'une population recombinante en Europe dite de “tête de pont”. Il est intéressant de noter que l'émergence de cette lignée clonale s'est accompagnée d'une transition évolutive d’une reproduction de type sexuée vers une reproduction asexuée au sein de ces populations. Enfin, dans le troisième chapitre, j'ai étudié les changements temporels de la diversité génétique de populations de <i>C. parasitica</i> établies dans le sud de la Suisse, ainsi que les liens potentiels entre la présence du mycovirus hyperparasitaire délétère Cryphonectria hypovirus 1 (CHV1) et la diversité du génome fongique. Les résultats indiquent une augmentation du niveau de recombinaison entre individus fongiques apparentés, entraînant une grande similitude génétique des génotypes et facilitant la transmission du mycovirus CHV1. Il n'y a pas eu de changements substantiels dans la structure de cette population fongique du sud de la Suisse, et aucun impact lié à la présence du CHV1 n’a été détecté sur la diversité du génome fongique durant une période d’environ 30 ans. Bien que nos résultats montrent une incidence stable du mycovirus CHV1 au sein des populations fongiques sur trois décennies, les dynamiques d'interaction à court terme sont probablement très volatiles. Les conclusions générales de cette thèse de doctorat soulignent la pertinence des déterminants génomiques qui facilitent l'émergence et les invasions d'agents pathogènes. <i>C. parasitica</i> est un modèle utile pour étudier les questions fondamentales de l'évolution des pathogènes et des processus invasifs, ainsi que les interactions antagonistes pathogènes-hyperparasites. <br>
<b>Abstract</b><br>Invasive pathogens are a threat to forest and agroecosystems, as well as animal and human health. Identifying genomic determinants of pathogen evolution, as well as investigations into the genetic structure of invasive pathogen populations provide fundamental insights to why species can emerge as invasive pathogens. In this PhD project I investigated the emergence and population genomics of the invasive chestnut blight fungus <i>Cryphonectria parasitica</i>, using comparative and population genomic approaches. <i>C. parasitica</i> recently emerged as an invasive bark pathogen on non-Asian <i>Castanea</i> species in North America and Europe. In the first chapter, I investigated genomic determinants of lifestyle transitions in the genus <i>Cryphonectria</i>, by genome comparisons of <i>C. parasitica</i> and its sister species. The study uncovered a striking loss of genes associated with carbohydrate metabolism in the invasive pathogen <i>C. parasitica</i>, which may have promoted its pathogenicity on <i>Castanea</i> species. The second chapter explores the emergence and diversification of a highly invasive chestnut blight lineage across south-eastern Europe. By analyzing the genome-wide diversity of a large set of <i>C. parasitica</i> isolates of predominantly European origin, the study showed that a highly successful clonal pathogen lineage can emerge from a recombinant bridgehead population within Europe. Interestingly, the emergence of this clonal lineage was accompanied by an evolutionary transition from mixed mating type populations to single mating type outbreak populations. Lastly, in the third chapter I investigated temporal changes in genetic diversity of established <i>C. parasitica</i> populations in southern Switzerland, as well as potential links between the presence of the deleterious hyperparasitic mycovirus Cryphonectria hypovirus 1 (CHV1) and fungal genome-wide diversity. The results indicate increased mating among related fungal individuals, resulting in high genetic similarity of genotypes and facilitated CHV1 transmission. There were no substantial changes in fungal population structure and after ˜30 years and no detectable impact of CHV1 presence on fungal genome-wide diversity. Although our results show stable CHV1 incidence in fungal populations over three decades, the short-term interaction dynamics are likely highly volatile. The overall findings of this PhD thesis highlight the relevance of genomic determinants facilitating pathogen emergence and invasions. <i>C. parasitica</i> is a useful model to study fundamental questions of pathogen evolution and invasive processes, as well as antagonistic pathogen-hyperparasite interactions.
<b>Abstract</b><br>Invasive pathogens are a threat to forest and agroecosystems, as well as animal and human health. Identifying genomic determinants of pathogen evolution, as well as investigations into the genetic structure of invasive pathogen populations provide fundamental insights to why species can emerge as invasive pathogens. In this PhD project I investigated the emergence and population genomics of the invasive chestnut blight fungus <i>Cryphonectria parasitica</i>, using comparative and population genomic approaches. <i>C. parasitica</i> recently emerged as an invasive bark pathogen on non-Asian <i>Castanea</i> species in North America and Europe. In the first chapter, I investigated genomic determinants of lifestyle transitions in the genus <i>Cryphonectria</i>, by genome comparisons of <i>C. parasitica</i> and its sister species. The study uncovered a striking loss of genes associated with carbohydrate metabolism in the invasive pathogen <i>C. parasitica</i>, which may have promoted its pathogenicity on <i>Castanea</i> species. The second chapter explores the emergence and diversification of a highly invasive chestnut blight lineage across south-eastern Europe. By analyzing the genome-wide diversity of a large set of <i>C. parasitica</i> isolates of predominantly European origin, the study showed that a highly successful clonal pathogen lineage can emerge from a recombinant bridgehead population within Europe. Interestingly, the emergence of this clonal lineage was accompanied by an evolutionary transition from mixed mating type populations to single mating type outbreak populations. Lastly, in the third chapter I investigated temporal changes in genetic diversity of established <i>C. parasitica</i> populations in southern Switzerland, as well as potential links between the presence of the deleterious hyperparasitic mycovirus Cryphonectria hypovirus 1 (CHV1) and fungal genome-wide diversity. The results indicate increased mating among related fungal individuals, resulting in high genetic similarity of genotypes and facilitated CHV1 transmission. There were no substantial changes in fungal population structure and after ˜30 years and no detectable impact of CHV1 presence on fungal genome-wide diversity. Although our results show stable CHV1 incidence in fungal populations over three decades, the short-term interaction dynamics are likely highly volatile. The overall findings of this PhD thesis highlight the relevance of genomic determinants facilitating pathogen emergence and invasions. <i>C. parasitica</i> is a useful model to study fundamental questions of pathogen evolution and invasive processes, as well as antagonistic pathogen-hyperparasite interactions.
Notes
Doctorat, Université de Neuchâtel, Institut de biologie
Publication type
doctoral thesis
