Whole genome sequencing elucidates the species-wide diversity and evolution of fungicide resistance in the early blight pathogen Alternaria solani

Early blight of potato is caused by the fungal pathogen Alternaria solani and is an increasing problemworldwide. The primary strategy to control the disease is applying fungicides such as succinatedehydrogenase inhibitors (SDHI). SDHI-resistant strains, showing reduced sensitivity to treatments,appeared in Germany in 2013, five years after the introduction of SDHIs. Two primary mutations in the SDHcomplex (SdhB-H278Y and SdhC-H134R) have been frequently found throughout Europe. How theseresistances arose and spread, and whether they are linked to other genomic features, remains unknown.We performed whole-genome sequencing for A. solani isolates from potato fields across Europe (Germany,Sweden, Belgium, and Serbia) to better understand the pathogen's genetic diversity in general andunderstand the development and spread of the genetic mutations that lead to SDHI resistance. We usedancestry analysis and phylogenetics to determine the genetic background of 48 isolates. The isolates can begrouped into 7 genotypes. These genotypes do not show a geographical pattern but appear spreadthroughout Europe. The Sdh mutations appear in different genetic backgrounds, suggesting they aroseindependently, and the observed admixtures might indicate a higher adaptive potential in the fungus thanpreviously thought.Our research gives insights into the genetic diversity of A. solani on a genome level. The mixed occurrenceof different genotypes and apparent admixture in the populations indicate higher genomic complexity thananticipated. The conclusion that SDHI tolerance arose multiple times independently has importantimplications for future fungicide resistance management strategies. These should not solely focus onpreventing the spread of isolates between locations but also on limiting population size and the selectivepressure posed by fungicides in a given field to avoid the rise of new mutations in other geneticbackgrounds.