Fair-weather friends. Sequential co-infection demonstrates priority effects in the outcome of Parastagonospora nodorum and Pyrenophora tritici-repentis polymicrobial foliar disease of wheat

In plant and animal pathosystems, the host is typically challenged by more than one pathogen simultaneously. Most pathosystem studies involve a single pathogen, but where multiple pathogens have been studied, synergy, antagonism and priority effects have frequently been detected. Parastagonospora nodorum and Pyrenophora tritici-repentis cause septoria nodorum blotch and tan spot of wheat, respectively. Field co-infection between these fungal pathogens is widely established, however interaction dynamics remain poorly understood. Using a newly developed digital PCR method, we studied co-infection in naturally infected wheat fields, inoculated field trials and, controlled environment artificial infections. Natural infection revealed a clear majority of symptomatic infections involved both pathogens, with host leaves resistant to both pathogens showing significantly higher disease and pathogen biomass under co-infection compared to single-species. Controlled inoculum field experiments showed P. tritici-repentis priority was most similar to natural and controlled mixed infection, suggesting P. tritici-repentis priority occurs in natural systems. Laboratory experiments showed that consecutive infection where P. tritici-repentis was followed by P. nodorum in a resistant host resulted in a significant increase in disease and biomass for both pathogens. When P. nodorum established on the host first, P. tritici-repentis colonisation was highly reduced regardless of host resistance in both controlled field studies and laboratory experiments. To our knowledge this is the first description of asymmetric priority effects overcoming host resistance in a plant pathosystem. Resistance breeding strategies evaluating single pathogen challenges may inadvertently select for cultivars vulnerable to sequential co-infection, necessitating integrated disease complex approaches for durable resistance development.