Host specialization in the fungal plant pathogen Zymoseptoria tritici
The three closely related plant pathogenic species Zymoseptoria tritici (synonym: Mycosphaerella graminicola), Z. pseudotritici and Z. ardabiliae are hemi-biotrophic, ascomycete fungi with different host ranges. Z. tritici emerged at the onset of agriculture and is specialized to its host Triticum a...
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|Summary:||The three closely related plant pathogenic species Zymoseptoria tritici (synonym: Mycosphaerella graminicola), Z. pseudotritici and Z. ardabiliae are hemi-biotrophic, ascomycete fungi with different host ranges. Z. tritici emerged at the onset of agriculture and is specialized to its host Triticum aestivum (bread wheat). In contrast Z. pseudotritici and Z. ardabiliae infect different wild grass species at the center of origin and diversification of the Zymoseptoria grass pathogens and are unable to infect wheat.
Accelerated evolution of single genes is a key feature of pathogen adaptation following a host shift. Genes under positive selection exhibit an elevated ratio of non-synonymous (replacement) mutations to synonymous (silent) mutations. A ratio above 1 is indicative of positive selection and these positively selected genes can be identified by comparative genome analyses of closely related species that infect different hosts. From a comparative genome study of Zymoseptoria species the four positively selected genes Zt80707, Zt89160, Zt103264, and Zt110804 were chosen without a priori information about gene function or structure.
In this study it was shown that the four selected genes are up-regulated in planta. The genes are not involved in axenic growth of Z. tritici as shown by an in vitro assay, supporting a pathogenicity related role of the four gene products. The virulence of Z. tritici on wheat was significantly reduced for the two deletion mutants (Zt80707 and Zt103264) and both showed an impaired development of the asexual fruiting bodies (pycnidia) on wheat.
The deletion of Zt89160 caused a hypervirulent reaction in wheat while the fourth mutant (Zt110804) showed no detectable change in virulence-phenotype. The protein Zt80707 was moreover shown to be exclusively secreted in Z. tritici indicating that positive selection in this protein most likely relates to a novel extracellular function. Adaptation to the host plant wheat was shown for the proteins Zt80707 and Zt89160 as both deletion phenotypes could not or only partially be restored when the genes in Z. tritici were replaced with their orthologs of Z. pseudotritici.
The presented results demonstrate that evolutionary predictions provide a strong tool for the identification of genes involved in host adaptation and pathogen development. In addition it was shown that adaptive evolution during host specialization also strongly affects non-secreted proteins without effector function (Zt89160, Zt103264, and Zt110804).|