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Transcriptional adaptation facilitates host specialization in a wheat pathogen

ABSTRACT: Host-pathogen co-evolutionary dynamics force microbial plant pathogens to constantly develop and adjust specific adaptations to thrive in their plant host, and therefore also act as strong drivers of divergence and speciation in pathogens. Factors that confer host specialization and determine host specificity are very diverse and range from molecular and morphological strategies to metabolic and reproductive adaptations. Identification of these key factors is a major goal in the study of pathogen evolution and may aid the development of sustainable crops and crop protection strategies. We here took a novel experimental approach and conducted comparative microscopy and transcriptome analyses of the closely related, recently diverged fungal pathogens Zymoseptoria tritici, Z. pseudotritici, and Z. ardabiliae that establish compatible and incompatible interactions with wheat. Although infections of the incompatible species induce plant defense response during invasion of stomatal openings, we found a highly conserved early-infection program among the three species. The transcriptional programs of the three pathogens are conserved to a large extent, as only 9.2% of the 8,885 orthologous genes are significantly differentially expressed during initial infection of wheat. The genes up-regulated in the compatible pathogen reflect adaptation to growth in wheat tissue e.g., by re-programming of fungal metabolism. In contrast, genes primarily involved in counteracting cell stress and damage are strongly induced in the incompatible species. Based on the species-specific gene expression profiles, we further identified nine candidate genes encoding putative effectors and host-specificity determinants in Z. tritici. These effectors are strongly induced in the compatible species and may interfere with host immune suppression. We also identify putative necrotrophic effectors which are induced at the onset of necrotrophic growth. Together, the results presented here indicate that host specialization has involved transcriptional adaptation of a relatively small number of genes. Our findings demonstrate the potential comparative analyses of compatible and incompatible infections present for identifying traits involved in pathogen evolution and host specialization.

ORGANISM(S): Zymoseptoria pseudotritici Zymoseptoria ardabiliae

PROVIDER: GSE237842 | GEO | 2023/07/25

REPOSITORIES: GEO

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Project description:Plants have evolved strong innate immunity mechanisms, but successful pathogens evade or suppress plant immunity via effectors delivered into the plant cell. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on Arabidopsis thaliana, and a genome sequence is available for isolate Emoy2. Here, we exploit the availability of genome sequences for Hpa and Arabidopsis to measure gene-expression changes in both Hpa and Arabidopsis simultaneously during infection. Using a high-throughput cDNA tag sequencing method, we reveal expression patterns of Hpa predicted effectors and Arabidopsis genes in compatible and incompatible interactions, and promoter elements associated with Hpa genes expressed during infection. By resequencing Hpa isolate Waco9, we found it evades Arabidopsis resistance gene RPP1 through deletion of the cognate recognized effector ATR1. Arabidopsis salicylic acid (SA)-responsive genes including PR1 were activated not only at early time points in the incompatible interaction but also at late time points in the compatible interaction. By histochemical analysis, we found that Hpa suppresses SA-inducible PR1 expression, specifically in the haustoriated cells into which host-translocated effectors are delivered, but not in non-haustoriated adjacent cells. Finally, we found a highly-expressed Hpa effector candidate that suppresses responsiveness to SA. As this approach can be easily applied to host-pathogen interactions for which both host and pathogen genome sequences are available, this work opens the door towards transcriptome studies in infection biology that should help unravel pathogen infection strategies and the mechanisms by which host defense responses are overcome. Three weeks old Arabidopsis (Col-0) plants were inoculated with either the avirulent isolate Emoy2 (incompatible interaction) or the virulent isolate Waco9 (compatible interaction) of Hpa, and infected plants were harvested at 1, 3 and 5 days post-inoculation (dpi) for total RNA extraction. mRNA profiles were generated by deep sequencing on Illumina GAIIx using EXPRSS tag-seq protocol. Each biological replicate set of samples were sequenced as one batch (biorep1, biorep2 and biorep3 in filenames) and each batch was sequenced in 4 individual Illumina flowcell lanes (lane1 to lane4 in filenames). Four sequecing lanes of each three biological repliates resulted in 12 sequencing libraries. Emoy2 1, 3 and 5 dpi samples and Waco9 1 dpi samples were made two different codes (lib1 and lib2 in filenames) to generate higher depth of sequencing data. Each biological replicate set of samples were sequenced as one batch and each batch was sequenced in 4 individual Illumina flowcell lanes. Four sequecing lanes of each three biological repliates resulted in 12 sequencing libraries. 'The unassigned read_*' samples are for 'nobarcode_biorep[x]_lanne[x].fq' file containing sequences unassigned to any barcode from respective bioreplicate sequencing lanes.

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Transcriptional adaptation facilitates host specialization in a wheat pathogen

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