Rapidly Evolving Genes Are Key Players in Host Specialization and Virulence of the Fungal Wheat Pathogen Zymoseptoria tritici (Mycosphaerella graminicola)
Autor: | Petra Happel, Stephan Poppe, Lena Dorsheimer, Eva H. Stukenbrock |
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Rok vydání: | 2015 |
Předmět: |
lcsh:Immunologic diseases. Allergy
Immunology Virulence Microbiology Genome Evolution Molecular Ascomycota Virology Genetics Molecular Biology Pathogen Gene lcsh:QH301-705.5 Triticum Plant Diseases Comparative genomics biology food and beverages biology.organism_classification Phenotype Plant Leaves lcsh:Biology (General) Mycosphaerella graminicola Host-Pathogen Interactions Parasitology Host adaptation lcsh:RC581-607 Research Article |
Zdroj: | PLoS Pathogens PLoS Pathogens, Vol 11, Iss 7, p e1005055 (2015) |
ISSN: | 1553-7374 |
Popis: | 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. Author Summary Zymoseptoria spp provides a unique model system to study the underlying genetics of host specialization of plant pathogens. Closely related Zymoseptoria species, including the prominent wheat pathogen Z. tritici, have recently specialized to distinct grass hosts. Positively selected substitutions have played a central role in the acquisition of new host specificities. We have identified a small set of genes showing signatures of positive selection. We demonstrate that three of these four candidate genes play an important role during host infection. Two mutants of Z. tritici were impaired in virulence; a third mutant showed a hypervirulent phenotype. New protein specificities not only include changes at the amino acid sequence level but also at the level of the protein structure. We conducted a gene replacement experiment to test if mutant phenotypes in Z. tritici could be complemented by the insertion of orthologous genes from the two closely related species Z. pseudotritici and Z. ardabiliae. For two genes, we confirm that the species-specific protein changes are essential for proper protein functioning in Z. tritici; key traits involved in the evolution of virulence and host specificity of this prominent pathogen can be characterized via a combination of evolutionary predictions and functional analyses. |
Databáze: | OpenAIRE |
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