Fair-Weather Friends: Sequential Coinfection 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 coinfection between these fungal pathogens is widely established, but interaction dynamics remain poorly understood. Using a newly developed digital PCR (dPCR) method, we studied coinfection in naturally infected wheat fields, inoculated field trials, and controlled environment artificial infections. Natural infection revealed that a clear majority of symptomatic infections involved both pathogens, with host leaves resistant to both pathogens showing significantly higher disease and pathogen biomass under coinfection compared with single species infection. Controlled inoculum field experiments showed P. tritici-repentis priority was most similar to natural and controlled mixed infection, suggesting that 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 colonization 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 coinfection, necessitating integrated disease complex approaches for durable resistance development.[Formula: see text] Copyright © 2026 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.