Divergent outcomes of direct conspecific pathogen strain interaction and plant co-infection suggest consequences for disease dynamics

Abstract

Plant diseases are often caused by co-infections of multiple pathogens with the potential to aggravate disease severity. In genetically diverse pathogen species, co-infections can also be caused by multiple strains of the same species. However, the outcome of such mixed infections by different conspecific genotypes is poorly understood. The interaction among pathogen strains with complex lifestyles outside and inside of the host are likely shaped by diverse traits including metabolic capacity and the ability to overcome host immune responses. To disentangle competitive outcomes among pathogen strains, we investigated the fungal wheat pathogen Zymoseptoria tritici. The pathogen infects wheat leaves in complex strain assemblies and highly diverse populations persist between growing seasons. We investigated a set of 14 genetically different strains collected from the same field to assess both competitive outcomes under culture conditions and on the host. Growth kinetics of co-cultured strains significantly deviated from single strain expectations indicating competitive exclusion depending on the strain genotype. We found similarly complex outcomes of lesion development on plant leaves following co-infections by the same pairs of strains. While some pairings suppressed overall damage to the host, other combinations exceeded expectations of lesion development based on single strain outcomes. Strain competition outcomes in absence of the host were poor predictors of outcomes on the host suggesting that the interaction with the plant immune system adds significant complexity. Intraspecific co-infection dynamics likely make important contributions to disease severity and need to be integrated for a more complete understanding of host-pathogen dynamics in the environment. ImportancePlants are often attacked by a multitude of pathogens simultaneously. Different pathogen species can either facilitate or constrain the colonization by other pathogen species. Hence, natural infections are often the outcome of complex interactions between pathogens. To what extent the simultaneous colonization of genetically different strains of the same pathogen species matters for disease outcomes remains largely unclear though. We assessed the outcome of interactions between strains of the fungal wheat pathogen Zymoseptoria tritici. In absence of the host, strains cultured in pairs were growing differently compared to strains cultured alone. When infecting wheat leaves either with single or pairs of strains, we found also highly variable outcomes. Importantly, interactions between strains outside of the host were only poorly explaining how strains would interact when on the host. This suggests that pathogen strains engage in complex interactions shaped by their environment. Understanding the nature of such interactions within pathogen species will improve our ability to manage crop plant infections in the wild.