Evolutionary history and variation in host range of three Stagonosporopsis species causing gummy stem blight of cucurbits

• Gummy stem blight of cucurbits is caused by three distinct Stagonosporopsis species.
• The species are S. cucurbitacearum (syn. Didymella bryoniae), S. caricae, and S. citrulli.
• S. caricae is ancestral to the two other lineages, which are sister species.
• In growth chamber experiments all three species were equally aggressive to cucurbits.
• Only S. caricae, a known papaya pathogen, was aggressive to papaya in experiments.

Recently diverged species may form complexes of morphologically similar, yet genetically distinct lineages that occur in overlapping geographic ranges and niches. Using a multilocus sequencing approach we discovered that gummy stem blight of cucurbits is caused by three genetically distinct species: Stagonosporopsis cucurbitacearum (syn. Didymella bryoniae), Stagonosporopsis citrulli, and Stagonosporopsis caricae, which had previously been considered only a pathogen of papaya. Experiments showed that all three species are pathogenic to cucurbits in the genera Cucurbita, Cucumis, and Citrullus, but only S. caricae is aggressive to papaya. Species tree estimates show that S. citrulli and S. cucurbitacearum are phylogenetically distinct sister species, and that S. caricae is the ancestral lineage. The time estimate for divergence of S. caricae from the ancestor of S. cucurbitacearum and S. citrulli at 72 900 YBP pre-dates domestication of papaya and Cucurbita species in the American tropics. The divergence estimate observed for S. cucurbitacearum and S. citrulli at 10 900 YBP suggests that diversification of Cucurbita species and domestication of gourds and squashes could have driven their divergence. This work highlights the use of molecular systematics and population genetics to elucidate genetic identity among previously unassociated fungi and to understand the patterns of pathogen diversification.