Northern corn leaf blight (NCLB) is an important leaf disease in maize (Zea mays) worldwide and is spreading into new areas with expanding maize cultivation, like Germany. Exserohilum turcicum, causal agent of NCLB, infects and colonizes leaf tissue and induces elongated necrotic lesions. Disease control is based on fungicide application and resistant cultivars displaying monogenic resistance. Symptom expression and resistance mechanisms differ in plants carrying different resistance genes. Therefore, histological studies and DNA quantification were performed to compare the pathogenesis of E. turcicum races in maize lines exhibiting compatible or incompatible interactions. Maize plants from the differential line B37 with and without resistance genes Ht1, Ht2, Ht3, and Htn1 were inoculated with either incompatible or compatible races (race 0, race 1 and race 23N) of E. turcicum. Leaf segments from healthy and inoculated plants were collected at five different stages of infection and disease development from penetration (0–1 days post inoculation - dpi), until full symptom expression (14–18 dpi). Symptoms of resistance responses conveyed by the different Ht genes considerably differed between Ht1 (necrotic lesions with chlorosis), Ht2 (chlorosis and small lesions), Ht3 (chlorotic spots) and Htn1 (no lesions or wilt-type lesions). In incompatible interactions, fungal DNA was only detected in very low amounts. At 10 dpi, DNA content was elevated in all compatible interactions. Histological studies with Chlorazol Black E staining indicated that E. turcicum formed appressoria and penetrated the leaf surface directly in both types of interaction. In contrast to incompatible interactions, however, the pathogen was able to penetrate into xylem vessels at 6 dpi in compatible interactions and strongly colonized the mesophyll at 12 dpi, which is considered the crucial process differentiating susceptible from resistant interactions. Following the distinct symptom expressions, resistance mechanisms conferred by Ht1, Ht2, Ht3, and Htn1 genes apparently are different. Lower disease levels and a delayed progress of infection in compatible interactions with resistant lines imply that maize R genes to E. turcicum are associated with or confer additional quantitative resistance.

Setosphaeria turcica is a major fungal pathogen of maize and causes the foliar disease Northern corn leaf blight (NCLB). It originates from tropical regions and expanded into Central Europe since the 1980s, simultaneously with a rapid increase of maize cultivation area in this region. To investigate evolutionary processes influencing the rapid expansion of S. turcica we sequenced 121 isolates from Central Europe, Western Europe and Kenya. Population genetic inference revealed five genetically distinct clusters that differ by their geographic distribution and emergence dates. One genetically diverse cluster is restricted to Kenya, and the four European clusters consist of three distinct clonal lineages with low genetic diversity and one genetically diverse cluster with several clonal sublineages. A comparison of two different coalescent models for genetic diversity in the most frequent and geographically widespread clonal lineage in Europe supported a model of neutral, strongly exponential population growth over models accounting for different types of selection. In contrast to Kenyan isolates, European isolates did not show sexual recombination despite the presence of both mating types MAT1-1 and MAT1-2 in Europe. Within clonal lineages phenotypic variation in virulence to different monogenic resistances likely originated from repeated de novo mutations in virulence genes of S. turcica. k-mer based association mapping between genetic clusters did not identify genomic regions associated with pathogen races but few genomic regions that are significantly differentiated between two clonal lineages and contain putative effector genes. Our results suggest that the rapid colonization of Europe by different clonal lineages of S. turcica was not driven by selection of virulent races but reflects a neutral demographic process of fast pathogen population growth fostered by a rapid expansion of the maize cultivation area in this region.

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Modern agricultural practices, climate change, and globalization foster the rapid spread of plant pathogens, such as the maize fungal pathogen Setosphaeria turcica, which causes Northern corn leaf blight and expanded into Central Europe during the twentieth century. To investigate the rapid expansion of S. turcica, we sequenced 121 isolates from Europe and Kenya. Population genomic inference revealed a single genetically diverse cluster in Kenya and three clonal lineages with low diversity, as well as one cluster of multiple clonal sublineages in Europe. Phylogenetic dating suggests that all European lineages originated through sexual reproduction outside Europe and were subsequently introgressed multiple times. Unlike isolates from Kenya, European isolates did not show sexual recombination, despite the presence of both MAT1-1 and MAT1-2 mating types. For the clonal lineages, coalescent model selection supported a selectively neutral model with strong exponential population growth, rather than models with pervasive positive selection caused by host defense resistance or environmental adaptation. Within clonal lineages, phenotypic variation in virulence to different monogenic resistances, which defines the pathogen races, suggests that these races may originate from repeated mutations in virulence genes. Association testing based on k-mers did not identify genomic regions linked to pathogen races, but it did uncover strongly differentiated genomic regions between clonal lineages, which harbor genes with putative roles in pathogenicity. In conclusion, the expansion and population growth of S. turcica in Europe are mainly driven by an expansion of the maize cultivation area and not by rapid adaptation.

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