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Abstract:
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.
