Evolution of sympatric host-specialized lineages of the fungal plant pathogen Zymoseptoria passerinii in natural ecosystems.

The barley disease Septoria Speckled Leaf Blotch, caused by the fungus Zymoseptoria passerinii, last appeared in North America in the early 2000s. Although rare in crops, field sampling of wild grasses in the Middle East revealed the disease persistence in wild barley. Identification of Z. passerinii in various wild barley species prompted us to examine genomic signatures of host specialization and trace the emergence of the domesticated-barley-infecting lineage. Furthermore, we applied virulence assays and confocal laser microscopy to evaluate whether the disease development differs between wild and domesticated barley. Wild- and domesticated-host-infecting populations have diverged, and phylogenetic relationships support the evolution of sympatric host-specialized lineages in wild hosts. Cross-virulence assays showed that Z. passerinii from domesticated hosts infect domesticated barley and its wild ancestor, Hordeum spontaneum. However, wild isolates from Iran did not infect domesticated barley. Wild and domesticated pathosystems have similar disease timing and progression, suggesting its persistence does not depend on a shorter period of incubation. The study supports that a wide range of hosts can foster the evolution of host-specialized lineages in sympatry and provide novel insights into the evolution of understudied fungal pathogens on wild hosts.