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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.

plos pathogens

Rapidly Evolving Genes Are Key Players in Host Specialization and Virulence of the Fungal Wheat Pathogen Zymoseptoria tritici (Mycosphaerella graminicola)