Emergence of sympatric host-specific lineages of the fungal plant pathogen Zymoseptoria passerinii in natural ecosystems

Abstract

O_LIThe barley disease Septoria Speckled Leaf Blotch, caused by the fungal pathogen Zymoseptoria passerinii, had its last outbreak in North America in the early 2000s. Although rare in agricultural settings, field sampling of wild grasses in the Middle East revealed the disease persistence in wild barley. C_LIO_LIIdentification of Z. passerinii in distinct wild barley species led us to investigate signatures of host specialization using genomics to address the mode of emergence by host tracking or host range expansion. Furthermore, we applied virulence assays and confocal laser microscopy to evaluate if the disease development differs between wild and domesticated barley. C_LIO_LIWild- and domesticated-host infecting populations have diverged, and phylogenetic relationships support the emergence of sympatric host-specific lineages. Cross-virulence assays showed that Zymoseptoria 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 in natural ecosystems might be tied to environmental conditions. C_LIO_LIThe study supports that a wide range of hosts can foster the emergence of host-specific lineages in sympatry and provide novel insights into the evolution of understudied fungal pathogens on wild crop relatives. C_LI