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Abraham, Leen Nanchira
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Abraham, Leen Nanchira
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- PublicationAccès librePopulation-level transposable element expression dynamics influence trait evolution in a fungal crop pathogen(2024-03-13T00:00:00Z)
; ; 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. - PublicationAccès libreGenome-wide expression QTL mapping reveals the highly dynamic regulatory landscape of a major wheat pathogen(2023-11-20T00:00:00Z)
; In agricultural ecosystems, outbreaks of diseases are frequent and pose a significant threat to food security. A successful pathogen undergoes a complex and well-timed sequence of regulatory changes to avoid detection by the host immune system; hence, well-tuned gene regulation is essential for survival. However, the extent to which the regulatory polymorphisms in a pathogen population provide an adaptive advantage is poorly understood. - PublicationRestriction temporaireEvolution of gene regulation within a fungal pathogen species(Neuchâtel : Université de Neuchâtel, 2023)
; ; Regulation of gene expression is essential for an organism as it helps to respond to environmental cues. Genetic variation in the gene regulatory elements can alter the gene regulatory network and generate a gene expression variation within species. Variation in gene expression can provide an adaptive advantage for the individuals in the population. Despite the evidence of gene expression variation observed among a few individuals in a population, we lack a genome-wide view of regulatory variation within a population and its contribution to the adaptation of an individual in a population. In this thesis, we studied the extent of genomic and epigenomic regulatory variation within a plant pathogen population and its adaptative potential emphasizing the major pathogenicity-related gene categories. In the first chapter, we generated a genome-wide map of regulatory polymorphism governing gene expression. We identified a major proportion of genes (65%) with a regulatory variation. Insertion and deletions have a higher effect on gene expression variation than SNPs. Different gene elements contribute disproportionally to gene expression variation with enrichment of regulatory variants upstream of the transcription start site, 5’ and 3’ untranslated region. Further investigation showed enrichment of regulatory variants for genes predicted to be essential for fungal pathogenesis (Candidate effector genes, secondary metabolite encoding genes) but with comparatively small effect size, suggesting a different layer of gene regulation such as epigenetic regulation. We also show that previously reported trait-associated SNPs in the pathogen are more likely to be a cis-regulatory variant of the neighboring gene that may contribute to phenotypic variation. The second chapter analyzed the transcriptional variation of different transposable element families at individual loci. We established the link of genomic defense to the activity of the TE loci and found that a repeat-induced point mutation is likely to be a regulatory variant for TE transcriptional activity. Our analysis also identified the significant contribution of transposable element insertion polymorphism in transcriptional variation and pathogenicity-related traits (Virulence and secondary metabolite production) of the pathogen. Comparatively low effect genetic regulatory variant observed with our eQTL mapping approach led us to explore the epigenome variation in the pathogen population. We generated a genome-wide profile of H3K27 repressive histone mark variation in the pathogen population. The pathogen population showed a highly variable epigenome profile for the genes important for pathogenicity emphasizing the significant contribution of epigenomic variation in individual-specific finetuned regulation of pathogenicity-related genes during host infection. Our study integrating genetic and epigenetic variation in a plant fungal pathogen provides a comprehensive overview of the complexity of gene regulation and the different gene regulatory mechanisms associated with different gene categories important for plant pathogenesis. - PublicationAccès libreGenome-wide association mapping reveals genes underlying population-level metabolome diversity in a fungal crop pathogen(2022)
; ; Abstract Background Fungi produce a wide range of specialized metabolites (SMs) involved in biotic interactions. Pathways for the production of SMs are often encoded in clusters of tightly arranged genes identified as biosynthetic gene clusters. Such gene clusters can undergo horizontal gene transfers between species and rapid evolutionary change within species. The acquisition, rearrangement, and deletion of gene clusters can generate significant metabolome diversity. However, the genetic basis underlying variation in SM production remains poorly understood. Results Here, we analyzed the metabolite production of a large population of the fungal pathogen of wheat, Zymoseptoria tritici. The pathogen causes major yield losses and shows variation in gene clusters. We performed untargeted ultra-high performance liquid chromatography-high resolution mass spectrometry to profile the metabolite diversity among 102 isolates of the same species. We found substantial variation in the abundance of the detected metabolites among isolates. Integrating whole-genome sequencing data, we performed metabolite genome-wide association mapping to identify loci underlying variation in metabolite production (i.e., metabolite-GWAS). We found that significantly associated SNPs reside mostly in coding and gene regulatory regions. Associated genes encode mainly transport and catalytic activities. The metabolite-GWAS identified also a polymorphism in the 3′UTR region of a virulence gene related to metabolite production and showing expression variation. Conclusions Taken together, our study provides a significant resource to unravel polymorphism underlying metabolome diversity within a species. Integrating metabolome screens should be feasible for a range of different plant pathogens and help prioritize molecular studies. - PublicationAccès libreHistone H3K27 Methylation Perturbs Transcriptional Robustness and Underpins Dispensability of Highly Conserved Genes in Fungi(2021)
; ; Jeffrey TownsendAbstractEpigenetic modifications are key regulators of gene expression and underpin genome integrity. Yet, how epigenetic changes affect the evolution and transcriptional robustness of genes remains largely unknown. Here, we show how the repressive histone mark H3K27me3 underpins the trajectory of highly conserved genes in fungi. We first performed transcriptomic profiling on closely related species of the plant pathogen Fusarium graminearum species complex. We determined transcriptional responsiveness of genes across environmental conditions to determine expression robustness. To infer evolutionary conservation, we used a framework of 23 species across the Fusarium genus including three species covered with histone methylation data. Gene expression variation is negatively correlated with gene conservation confirming that highly conserved genes show higher expression robustness. In contrast, genes marked by H3K27me3 do not show such associations. Furthermore, highly conserved genes marked by H3K27me3 encode smaller proteins, exhibit weaker codon usage bias, higher levels of hydrophobicity, show lower intrinsically disordered regions, and are enriched for functions related to regulation and membrane transport. The evolutionary age of conserved genes with H3K27me3 histone marks falls typically within the origins of the Fusarium genus. We show that highly conserved genes marked by H3K27me3 are more likely to be dispensable for survival during host infection. Lastly, we show that conserved genes exposed to repressive H3K27me3 marks across distantly related Fusarium fungi are associated with transcriptional perturbation at the microevolutionary scale. In conclusion, we show how repressive histone marks are entangled in the evolutionary fate of highly conserved genes across evolutionary timescales. - PublicationAccès libreA 19-isolate reference-quality global pangenome for the fungal wheat pathogen Zymoseptoria tritici(2020)
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