Fair-weather friends: Priority determines disease outcomes in an agonistic multi-pathogen crop pathosystem

In both plant and animal pathosystems, the host is typically challenged by
more than one pathogen simultaneously. Parastagonospora nodorum and
Pyrenophora tritici-repentis frequently co-infect the same leaves, yet
their interaction dynamics remain poorly understood due to limitations in
species-specific pathogen quantification. We investigated how arrival
order and host resistance affect disease outcomes during co-infection. We
developed a duplex digital PCR assay targeting single copy α-tubulin genes
to enable directly comparable biomass quantification of both pathogens.
Field surveys and controlled sequential inoculation experiments were
conducted across wheat cultivars with differential resistance to evaluate
priority effects on pathogen proliferation and disease severity. Field
surveys revealed a clear majority of symptomatic infections involved both
pathogens, with individual pathogen biomass significantly elevated under
co-infection, particularly in moderately resistant cultivars. Sequential
inoculation experiments revealed asymmetric priority effects: P.
tritici-repentis establishment facilitated subsequent P. nodorum
colonisation and overcame host resistance, while P. nodorum priority
consistently suppressed P. tritici-repentis regardless of host genotype.
These asymmetric priority effects demonstrate that pathogen arrival order
fundamentally alters disease dynamics and can overcome genetic resistance.
Current resistance breeding strategies evaluating single-pathogen
challenges may inadvertently select cultivars vulnerable to sequential
co-infection, necessitating integrated disease complex approaches for
durable resistance development.