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A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements.

ABSTRACT: Fungal pathogens can rapidly evolve virulence towards resistant crops in agricultural ecosystems. Gains in virulence are often mediated by the mutation or deletion of a gene encoding a protein recognized by the plant immune system. However, the loci and the mechanisms of genome evolution enabling rapid virulence evolution are poorly understood. We performed genome-wide association mapping on a global collection of 106 strains of Zymoseptoria tritici, the most damaging pathogen of wheat in Europe, to identify polymorphisms linked to virulence on two wheat varieties. We found 25 distinct genomic loci associated with reproductive success of the pathogen. However, no locus was shared between the host genotypes, suggesting host specialization. The main locus associated with virulence encoded a highly expressed, small secreted protein. Population genomic analyses showed that the gain in virulence was explained by a segregating gene deletion polymorphism. The deletion was likely adaptive by preventing detection of the encoded protein. Comparative genomics of closely related species showed that the locus emerged de novo since speciation. A large cluster of transposable elements in direct proximity to the locus generated extensive rearrangements leading to multiple independent gene losses. Our study demonstrates that rapid turnover in the chromosomal structure of a pathogen can drive host specialization.

SUBMITTER: Hartmann FE

PROVIDER: S-EPMC5437930 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements.

Hartmann Fanny E FE Sánchez-Vallet Andrea A McDonald Bruce A BA Croll Daniel D

The ISME journal 20170124 5

Fungal pathogens can rapidly evolve virulence towards resistant crops in agricultural ecosystems. Gains in virulence are often mediated by the mutation or deletion of a gene encoding a protein recognized by the plant immune system. However, the loci and the mechanisms of genome evolution enabling rapid virulence evolution are poorly understood. We performed genome-wide association mapping on a global collection of 106 strains of Zymoseptoria tritici, the most damaging pathogen of wheat in Europe ...[more]

PMID: 28117833

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Project description: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.

Project description:The speciation of pathogens can be driven by divergent host specialization. Specialization to a new host is possible via the acquisition of advantageous mutations fixed by positive selection. Comparative genome analyses of closely related species allows for the identification of such key substitutions via inference of genome-wide signatures of positive selection. We previously used a comparative genomics framework to identify genes that have evolved under positive selection during speciation of the prominent wheat pathogen Zymoseptoria tritici (synonym Mycosphaerella graminicola). In this study, we conducted functional analyses of four genes exhibiting strong signatures of positive selection in Z. tritici. We deleted the four genes in Z. tritici and confirm a virulence-related role of three of the four genes ΔZt80707, ΔZt89160 and ΔZt103264. The two mutants ΔZt80707 and ΔZt103264 show a significant reduction in virulence during infection of wheat; the ΔZt89160 mutant causes a hypervirulent phenotype in wheat. Mutant phenotypes of ΔZt80707, ΔZt89160 and ΔZt103264 can be restored by insertion of the wild-type genes. However, the insertion of the Zt80707 and Zt89160 orthologs from Z. pseudotritici and Z. ardabiliae do not restore wild-type levels of virulence, suggesting that positively selected substitutions in Z. tritici may relate to divergent host specialization. Interestingly, the gene Zt80707 encodes also a secretion signal that targets the protein for cell secretion. This secretion signal is however only transcribed in Z. tritici, suggesting that Z. tritici-specific substitutions relate to a new function of the protein in the extracellular space of the wheat-Z. tritici interaction. Together, the results presented here highlight that Zt80707, Zt103264 and Zt89160 represent key genes involved in virulence and host-specific disease development of Z. tritici. Our findings illustrate that evolutionary predictions provide a powerful tool for the identification of novel traits crucial for host adaptation and pathogen evolution.

Dataset Information

A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements.

Publications

A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements.

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