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Rapid evolution in a plant-pathogen interaction and the consequences for introduced host species.

ABSTRACT: Plant species introduced into new regions can both leave behind co-evolved pathogens and acquire new ones. Traits important to infection and virulence are subject to rapid evolutionary change in both plant and pathogen. Using Stemphylium solani, a native foliar necrotroph on clovers (Trifolium and Medicago) in California, USA, we explore how plant-fungal interactions may change in an invasion context. After four generations of experimental serial passage through multiple hosts, Stemphylium consistently showed increased infection rates but no consistent change in damage to the host. In a historical opportunity study, we compared infection and virulence across four groups of clover hosts: California natives, European clovers not found in California, and both California and European genotypes of species naturalized in California. There was significant variation among hosts, but no pattern across the four groups. However, in direct comparisons of familiar California genotypes to unfamiliar European genotypes of the same naturalized species, Stemphylium consistently infected familiar hosts more frequently, while causing less damage on them. This pattern is consistent with the hypothesis of adaptive evolution in both the pathogen (ability to infect) and the host (tolerance of infection). Together these results suggest the potential for rapid evolution to alter interactions between plant invaders and their natural enemies.

SUBMITTER: Gilbert GS

PROVIDER: S-EPMC3352484 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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Rapid evolution in a plant-pathogen interaction and the consequences for introduced host species.

Gilbert Gregory S GS Parker Ingrid M IM

Evolutionary applications 20100301 2

Plant species introduced into new regions can both leave behind co-evolved pathogens and acquire new ones. Traits important to infection and virulence are subject to rapid evolutionary change in both plant and pathogen. Using Stemphylium solani, a native foliar necrotroph on clovers (Trifolium and Medicago) in California, USA, we explore how plant-fungal interactions may change in an invasion context. After four generations of experimental serial passage through multiple hosts, Stemphylium consi ...[more]

PMID: 25567915

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Project description: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 cocultured strains (~100 pairs) 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 the 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 outcomes in the wild. IMPORTANCE Plants are often attacked by a multitude of pathogens simultaneously, and different species can facilitate or constrain the colonization by others. To what extent simultaneous colonization by different strains of the same species matters, remains unclear. We focused on intra-specific interactions between strains of the major fungal wheat pathogen Zymoseptoria tritici. The pathogen persists in the environment before infecting plant leaves early in the growing season. Leaves are typically colonized by a multitude of strains. Strains cultured in pairs without host were growing differently compared to strains cultured alone. Wheat leaves infected either with single or pairs of strains, we found also highly variable outcomes. Interactions between strains outside of the host were only poorly explaining how strains would interact when on the host, suggesting that pathogen strains engage in complex interactions dependent on the environment. Better understanding within-species interactions will improve our ability to manage crop infections.

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Rapid evolution in a plant-pathogen interaction and the consequences for introduced host species.

Publications

Rapid evolution in a plant-pathogen interaction and the consequences for introduced host species.

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