Evolution of gene regulation within a fungal pathogen species

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.

Jury composé comme suit:
Prof. Daniel Croll, directeur de thèse, Université de Neuchâtel, Suisse
Prof. Pilar Junier, Université de Neuchâtel, Suisse
Prof. Juliette de Meaux, Universität zu Köln, Allemagne
Soutenue à Neuchâtel, le 23 mai 2023