Abstract
Leptosphaeria maculans ‘brassicae’ (Lmb) and Leptosphaeria maculans ‘lepidii’ (Lml) are closely related phytopathogenic species that exhibit a large macrosynteny but contrasting genome structure. Lmb has more than 30% of repeats clustered in large repeat-rich regions, while the Lml genome has only a small amount of evenly distributed repeats. Repeat-rich regions of Lmb are enriched in effector genes, expressed during plant infection. The distinct genome structures of Lmb and Lml provide an excellent model for comparing the organization of pathogenicity genes in relation to the chromatin landscape in two closely related phytopathogenic fungi. Here, we performed chromatin immunoprecipitation (ChIP) during axenic culture, targeting histone modifications typical for heterochromatin or euchromatin, combined with transcriptomic analysis to analyze the influence of chromatin organization on gene expression. In both species, we found that facultative heterochromatin is enriched with genes lacking functional annotation, including numerous effector and species-specific genes. Notably, orthologous genes located in H3K27me3 domains are enriched with effector genes. Compared to other fungal species, including Lml, Lmb is distinct in having large H3K9me3 domains associated with repeat-rich regions that contain numerous species-specific effector genes. Discovery of these two distinctive heterochromatin landscapes now raises questions about their involvement in the regulation of pathogenicity, the dynamics of these domains during plant infection and the selective advantage to the fungus to host effector genes in H3K9me3 or H3K27me3 domains.
Highlights
Each year, hundreds of millions of tons of agricultural crops are devastated by plant pathogenic fungi or made unfit for consumption due to contamination by mycotoxins (Fisher et al 2018)
Mapping of the chromatin immunoprecipitation (ChIP)-seq data was followed by identification of significantly enriched domains, for any of the histone modifications targeted, and reproducibility of the biological replicates was assessed (Supplementary Tables 2 and 3)
We identified a positive correlation between the location of transposable elements (TE) and H3K9me3 domains (Kendall’s Ƭ: 0.87 and 0.68, P < 2.2.10−16 for Leptosphaeria maculans ‘brassicae’ (Lmb) and Leptosphaeria maculans ‘lepidii’ (Lml) respectively; Figs. 2, 3, and 4; Supplementary Figure 1; Tables 1 and 2) and between the location of coding sequences (CDS) and H3K4me2 (Kendall’s Ƭ: 0.55 and 0.25, P < 2.2.10−16 for Lmb and Lml respectively; Figs. 2, 3, and 4; Supplementary Figure 1; Tables 1 and 2)
Summary
Hundreds of millions of tons of agricultural crops are devastated by plant pathogenic fungi or made unfit for consumption due to contamination by mycotoxins (Fisher et al 2018). Fungal plant pathogens have proven capable of rapidly evolving resistance against fungicides (Fisher et al 2018) and to overcome specific plant resistance genes within a few years (for instance in Leptosphaeria maculans; Rouxel and Balesdent 2017), emphasizing the need for improved control methods. Plants have evolved strategies to recognize and counteract effectors, exposing them to a strong selection pressure by the host immune system (Stergiopoulos et al 2007; Chuma et al 2011; Rouxel and Balesdent 2017). In the course of the coevolution between a pathogen and its host, the host has developed an active immune system allowing the direct or indirect recognition of some effector molecules, to activate defence responses, often involving a local cell death, called the hypersensitive response. Effectors that can be recognized by the host are called avirulence proteins (Jones and Dangl 2006)
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