SnToxA, SnTox1 and SnTox3 originated in Parastagonospora nodorum in the Fertile Crescent

Abstract

The center of origin of the globally distributed wheat pathogen Parastagnospora nodorum has remained uncertain because only a small number of isolates from the Fertile Crescent, a region in the Middle East where wheat was domesticated from wild grasses, were included in earlier population genetic and phylogeographic studies. We isolated and genetically analyzed 193 P. nodorum strains from three naturally infected wheat fields distributed across Iran, a country located within the Fertile Crescent, using eleven neutral microsatellite loci. Compared to previous studies that included populations from North America, Europe, Africa, Australia and China, the populations from Iran had the highest genetic diversity globally and also exhibited greater population structure over smaller spatial scales, patterns typically associated with a species center of origin. Genes encoding the necrotrophic effectors SnToxA, SnTox1 and SnTox3 were found at a high frequency in the Iranian population. By sequencing 96 randomly chosen Iranian strains, we detected new alleles for all three effector genes. Analyses of allele diversity showed that all three effector genes had higher diversity in Iran than in any population included in previous studies, with Iran acting as a hub for the effector diversity that was found in other global populations. Taken together, these findings support the hypothesis that P. nodorum originated either within or nearby the Fertile Crescent with a genome that already encoded all three necrotrophic effectors during its emergence as a pathogen on wheat. Our findings also suggest that P. nodorum was the original source of the ToxA genes discovered in the wheat pathogens Phaeosphaeria avenaria f. sp. tritici 1, Pyrenophora tritici-repentis and Bipolaris sorokiniana.