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  • Publication
    Accès libre
    Population-level transposable element expression dynamics influence trait evolution in a fungal crop pathogen
    The rapid adaptive evolution of microbes is driven by strong selection pressure acting on genetic variation. How adaptive genetic variation is generated within species and how such variation influences phenotypic trait expression is often not well understood though. We focused on the recent activity of transposable elements (TEs) using deep population genomics and transcriptomics analyses of a fungal plant pathogen with a highly active content of TEs in the genome. causes one of the most damaging diseases on wheat, with recent adaptation to the host and environment being facilitated by TE-associated mutations. We obtained genomic and RNA-sequencing data from 146 isolates collected from a single wheat field. We established a genome-wide map of TE insertion polymorphisms in the population by analyzing recent TE insertions among individuals. We quantified the locus-specific transcription of individual TE copies and found considerable population variation at individual TE loci in the population. About 20% of all TE copies show transcription in the genome suggesting that genomic defenses such as repressive epigenetic marks and repeat-induced polymorphisms are at least partially ineffective at preventing the proliferation of TEs in the genome. A quarter of recent TE insertions are associated with expression variation of neighboring genes providing broad potential to influence trait expression. We indeed found that TE insertions are likely responsible for variation in virulence on the host and potentially diverse components of secondary metabolite production. Our large-scale transcriptomics study emphasizes how TE-derived polymorphisms segregate even in individual microbial populations and can broadly underpin trait variation in pathogens.IMPORTANCEPathogens can rapidly adapt to new hosts, antimicrobials, or changes in the environment. Adaptation arises often from mutations in the genome; however, how such variation is generated remains poorly understood. We investigated the most dynamic regions of the genome of a major fungal pathogen of wheat. We focused on the transcription of transposable elements. A large proportion of the transposable elements not only show signatures of potential activity but are also variable within a single population of the pathogen. We find that this variation in activity is likely influencing many important traits of the pathogen. Hence, our work provides insights into how a microbial species can adapt over the shortest time periods based on the activity of transposable elements.
  • Publication
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    A systematic screen for co-option of transposable elements across the fungal kingdom
    How novel protein functions are acquired is a central question in molecular biology. Key paths to novelty include gene duplications, recombination or horizontal acquisition. Transposable elements (TEs) are increasingly recognized as a major source of novel domain-encoding sequences. However, the impact of TE coding sequences on the evolution of the proteome remains understudied. Here, we analyzed 1237 genomes spanning the phylogenetic breadth of the fungal kingdom. We scanned proteomes for evidence of co-occurrence of TE-derived domains along with other conventional protein functional domains. We detected more than 13,000 predicted proteins containing potentially TE-derived domain, of which 825 were identified in more than five genomes, indicating that many host-TE fusions may have persisted over long evolutionary time scales. We used the phylogenetic context to identify the origin and retention of individual TE-derived domains. The most common TE-derived domains are helicases derived from Academ, Kolobok or Helitron. We found putative TE co-options at a higher rate in genomes of the Saccharomycotina, providing an unexpected source of protein novelty in these generally TE depleted genomes. We investigated in detail a candidate host-TE fusion with a heterochromatic transcriptional silencing function that may play a role in TE and gene regulation in ascomycetes. The affected gene underwent multiple full or partial losses within the phylum. Overall, our work establishes a kingdom-wide view of putative host-TE fusions and facilitates systematic investigations of candidate fusion proteins.
  • Publication
    Accès libre
    Recent transposable element bursts are associated with the proximity to genes in a fungal plant pathogen
    The activity of transposable elements (TEs) contributes significantly to pathogen genome evolution. TEs often destabilize genome integrity but may also confer adaptive variation in pathogenicity or resistance traits. De-repression of epigenetically silenced TEs often initiates bursts of transposition activity that may be counteracted by purifying selection and genome defenses. However, how these forces interact to determine the expansion routes of TEs within a pathogen species remains largely unknown. Here, we analyzed a set of 19 telomere-to-telomere genomes of the fungal wheat pathogenZymoseptoria tritici. Phylogenetic reconstruction and ancestral state estimates of individual TE families revealed that TEs have undergone distinct activation and repression periods resulting in highly uneven copy numbers between genomes of the same species. Most TEs are clustered in gene poor niches, indicating strong purifying selection against insertions near coding sequences, or as a consequence of insertion site preferences. TE families with high copy numbers have low sequence divergence and strong signatures of defense mechanisms (i.e., RIP). In contrast, small non-autonomous TEs (i.e., MITEs) are less impacted by defense mechanisms and are often located in close proximity to genes. Individual TE families have experienced multiple distinct burst events that generated many nearly identical copies. We found that aCopiaelement burst was initiated from recent copies inserted substantially closer to genes compared to older copies. Overall, TE bursts tended to initiate from copies in GC-rich niches that escaped inactivation by genomic defenses. Our work shows how specific genomic environments features provide triggers for TE proliferation in pathogen genomes.
  • Publication
    Accès libre
    The role of transposable elements in the adaptive evolution of fungi
    (Neuchâtel, 2022)
    Les éléments transposables (ETs) sont des éléments génétiques répétitifs et mobiles. Les ET autonomes contiennent toutes les séquences codantes nécessaires à leur excision, duplication et insertion. Les ET peuvent être considérés comme des éléments égoïstes ou des parasites génomiques, ayant le potentiel de dramatiquement perturber le génome par l’interruption de gènes, la délétion de séquences ou la modification de l'expression des gènes. Cependant, ces perturbations peuvent également offrir de nouvelles fonctions avantageuses. Des recherches récentes ont souligné les fonctions bénéfiques de certaines insertions d’ET, d’augmenter l'adaptabilité à de nouvelles conditions environnementales ou à des impacts toxiques, ou prenant part au protéome. Dans cette thèse, nous avons étudié comment les ET influencent les espèces fongiques, d'un impact local et à court terme à des échelles de temps évolutives plus profondes, et comment les ETs eux-mêmes évoluent sous des processus neutres et sélectifs. Dans le premier chapitre, nous avons étudié la dynamique des populations et l'impact des ETs sur l'évolution de la taille du génome chez un champignon phytopathogène. Malgré un fort impact de la sélection négative sur les ET, nous avons détecté une augmentation du nombre de copies entre la population d'origine et les populations plus récemment établies, avec une forte augmentation récente en Amérique du Nord. L'augmentation du nombre de copies de ET est également fortement corrélée à une augmentation de la taille du génome. Cependant, il n'est pas clair quels ETs conduisent à une augmentation de leur nombre de copies, et où les copies actives s'insèrent. Dans un deuxième chapitre, nous avons donc étudié les voies d'expansion des ETs dans plusieurs génomes de haute qualité. Nous avons constaté que les ET les plus anciens s'accumulent dans les régions avec peu de gènes et une forte indication de mécanismes de défense contre les ET. À l’inverse, les insertions les plus récentes sont généralement situées plus près de gènes et ne sont pas encore affectées par les mécanismes de défense. Pour étudier l'impact des ETs sur l'évolution du protéome, nous avons dans un troisième chapitre porté nos études sur un ensemble d’espèces couvrant le règne des champignons. Nous avons identifié les protéines qui chez ces différentes espèces présentent les indications d’une fusion entre protéines hôte et ET. Nous avons trouvé une accumulation de fusions hôte-ET chez la sous-classe des Saccharomycotina, qui de façon générale ont un faible nombre de gènes et d’ETs. La majorité des fusions hôte-ET possède un domaine hélicase, indiquant un fort impact des fonctions de liaison à l'ADN. De plus, nous avons trouvé plusieurs fusions hôte-ET qui sont potentiellement impliquées dans des mécanismes de défense contre les ET.
    Abstract Transposable elements (TEs) are repetitive and mobile genetic elements. Autonomous TEs contain all coding regions needed for excision, duplication and insertion. TEs can be considered to be selfish elements or genomic parasites, with the potential to dramatically disturb the genome by gene disruption, deletion of regions or change in gene expression. However, dramatic distortion also carries the potential to provide beneficial new functions. An increasing body of research highlights beneficial impacts of TE insertions that increase adaptability to new environmental conditions or toxic impacts, or become part of the proteome. In this thesis, we studied how TEs influence fungal species from a local and short-term impact to deeper evolutionary time scales, and how TEs themselves are evolving. In the first chapter, we studied population dynamics and the impact of TEs on genome size evolution in a fungal plant pathogen. Despite a strong impact of purifying selection, we detected an increase in TE copies from the population of origin to more recently established populations, with a strong recent burst in North America. Increase in TE copy numbers is strongly correlated with an increase in genome size as well. Yet, which TEs lead to a copy number increase, and where active copies insert was not clear. We therefore studied expansion routes of TEs in a number of high-quality genomes in the second chapter. We found that older elements are accumulated in regions with low gene contents and high indication of an ascomycete-specific defense mechanisms against TEs. Insertions that are part of a recent burst are generally closer located to genes and not yet affected by defense mechanisms. To study the impact of TEs on the proteome evolution, we analyzed species covering the fungal kingdom in the third chapter. We screened for proteins with indications to be host-TE fusions. We found an accumulation of host-TE fusions in Saccharomycotina that generally have a lower gene- and TE content. The majority of host-TE fusions has a helicase TE domain, indicating a strong impact of DNA binding functions. Furthermore, we found several host-TE fusions that are potentially involved in defense mechanisms against TEs.
  • Publication
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  • Publication
    Accès libre
    High-quality genome assembly of Pseudocercospora ulei the main threat to natural rubber trees
    (2022)
    Sandra González-Sayer
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    ;
    Ibonne García
    ;
    Fabio Aristizabal
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    ;
    Diego M. Riaño-Pachon
  • Publication
    Accès libre
    The population genetics of adaptation through copy number variation in a fungal plant pathogen
    (2022) ; ;
    Norfarhan Mohd‐Assaad
    ;
    AbstractMicrobial pathogens can adapt rapidly to changing environments such as the application of pesticides or host resistance. Copy number variations (CNVs) are a major source of adaptive genetic variation for recent adaptation. Here, we analyse how a major fungal pathogen of barley, Rhynchosporium commune, has adapted to the host environment and fungicide applications. We screen the genomes of 125 isolates sampled across a worldwide set of populations and identify a total of 7,879 gene duplications and 116 gene deletions. Most gene duplications result from segmental chromosomal duplications. Although CNVs are generally under negative selection, we find that genes affected by CNVs are enriched in functions related to host exploitation (i.e., effectors and cell‐wall‐degrading enzymes). We perform genome‐wide association studies (GWAS) and identify a large segmental duplication of CYP51A that has contributed to the emergence of azole resistance and a duplication encompassing an effector gene affecting virulence. We show that the adaptive CNVs were probably created by recently active transposable element families. Moreover, we find that specific transposable element families are important drivers of recent gene CNV. Finally, we use a genome‐wide single nucleotide polymorphism data set to replicate the GWAS and contrast it with the CNV‐focused analysis. Together, our findings show how extensive segmental duplications create the raw material for recent adaptation in global populations of a fungal pathogen.
  • Publication
    Accès libre
    A 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici
    Abstract Background The gene content of a species largely governs its ecological interactions and adaptive potential. A species is therefore defined by both core genes shared between all individuals and accessory genes segregating presence-absence variation. There is growing evidence that eukaryotes, similar to bacteria, show intra-specific variability in gene content. However, it remains largely unknown how functionally relevant such a pangenome structure is for eukaryotes and what mechanisms underlie the emergence of highly polymorphic genome structures. Results Here, we establish a reference-quality pangenome of a fungal pathogen of wheat based on 19 complete genomes from isolates sampled across six continents. Zymoseptoria tritici causes substantial worldwide losses to wheat production due to rapidly evolved tolerance to fungicides and evasion of host resistance. We performed transcriptome-assisted annotations of each genome to construct a global pangenome. Major chromosomal rearrangements are segregating within the species and underlie extensive gene presence-absence variation. Conserved orthogroups account for only ~ 60% of the species pangenome. Investigating gene functions, we find that the accessory genome is enriched for pathogenesis-related functions and encodes genes involved in metabolite production, host tissue degradation and manipulation of the immune system. De novo transposon annotation of the 19 complete genomes shows that the highly diverse chromosomal structure is tightly associated with transposable element content. Furthermore, transposable element expansions likely underlie recent genome expansions within the species. Conclusions Taken together, our work establishes a highly complex eukaryotic pangenome providing an unprecedented toolbox to study how pangenome structure impacts crop-pathogen interactions.