Highly flexible infection programs in a specialized wheat pathogen

Abstract

Many filamentous plant pathogens exhibit high levels of genomic variability, yet the impact of this variation on host–pathogen interactions is largely unknown. We have addressed host specialization in the wheat pathogen Zymoseptoria tritici. Our study builds on comparative analyses of infection and gene expression phenotypes of three isolates and reveals the extent to which genomic variation translates into phenotypic variation. The isolates exhibit genetic and genomic variation but are similarly virulent. By combining confocal microscopy, disease monitoring, staining of ROS, and comparative transcriptome analyses, we conducted a detailed comparison of the infection processes of these isolates in a susceptible wheat cultivar. We characterized four core infection stages: establishment, biotrophic growth, lifestyle transition, and necrotrophic growth and asexual reproduction that are shared by the three isolates. However, we demonstrate differentiated temporal and spatial infection development and significant differences in the expression profiles of the three isolates during the infection stages. More than 20% of the genes were differentially expressed and these genes were located significantly closer to transposable elements, suggesting an impact of epigenetic regulation. Further, differentially expressed genes were enriched in effector candidates suggesting that isolate‐specific strategies for manipulating host defenses are present in Z. tritici. We demonstrate that individuals of a host‐specialized pathogen have highly differentiated infection programs characterized by flexible infection development and functional redundancy. This illustrates how high genetic diversity in pathogen populations results in highly differentiated infection phenotypes, which fact needs to be acknowledged to understand host–pathogen interactions and pathogen evolution.

The transcription factor Zt107320 affects the dimorphic switch, growth and virulence of the fungal wheat pathogen Zymoseptoria tritici

“…a). In contrast, Z. tritici successfully infected and colonized the mesophyll tissue of the susceptible wheat cultivar Obelisk during different infection stages, as already described in detail (Haueisen et al , ). Penetration of leaf stomata at 4 dpi was followed by the establishment of a hyphal network in the mesophyll tissue until 7–11 dpi and subsequently the switch to necrotrophy when biomass increased substantially, resulting in the formation of pycnidia (Fig.…”

“…Data from Haueisen et al . (). (d) In planta expression of Zt107320 is displayed relative to expression during axenic growth.…”

“…Based on RT‐qPCR data we observed that Zt107320 is differentially expressed between non‐host and host infections and is further highly expressed during infections of compatible hosts. Although previous RNA‐Seq‐based transcriptome studies found Zt107320 to be expressed at different relative levels compared to liquid culture, both studies showed that it is up‐regulated during later stages of wheat infection and associated with necrotrophic host colonization, indicating a possible function for pycnidia formation (Haueisen et al , ; Rudd et al , ). Together, these findings support a role of Zt107320 in regulation of growth and pathogenicity of Z. tritici .…”

“…b). During the course of the infection of a compatible host, a separate study based on transcriptome data showed that the expression of Zt107320 increases over time, with the highest expression at 20 dpi (Haueisen et al , ). This expression pattern is consistent with a putative role of Zt107320 in growth regulation (Fig.…”

Evolution and plasticity of the transcriptome under temperature fluctuations in the fungal plant pathogen Zymoseptoria tritici

“…Indeed our results confirmed that a large region of 800kb on the chromosome 7 is without any transcriptional activity ( Additional file 3: Figure S5 ). This feature was already mentioned for the strain IPO-323 by (Rudd et al 2015; Schotanus et al 2015; and Haueisen et al 2019). This chromosomal region is marked with histone H3K27me3 modifications that mediate transcriptional silencing, and these epigenetic marks are similar to the marks already identified on ACs.…”