Asexual reproductive potential trumps virulence as a predictor of competitive ability in mixed infections

Bernasconi, Alessio; Alassimone, Julien; McDonald, Bruce A.; Sánchez‐Vallet, Andrea

doi:10.1111/1462-2920.16018

Cited by 8 publications

(20 citation statements)

References 49 publications

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“…of a strain-specific discriminant qPCR or fluorescent labelling techniques. A recent study of four fluorescence-tagged Z. tritici strains showed a consistent pattern of fast-growing strains also growing well in co-culture (25), however expanding both labelling and qPCR approaches to much larger pair collections as in this study will be challenging. How fungi recognize self from non-self at different morphological stages and under different environmental conditions remains poorly understood though.…”

Section: Discussionmentioning

confidence: 87%

“…During the infection process, Z. tritici produces hyphae that enter the intercellular space of wheat cells to produce pycnidia in the substomatal space (41, 42). Fluorescent microscopy analyses of co-infections showed that both hyphae and pycnidia are densely packed without apparent exclusion zones among genotypes (25). Increased damage to the host during co-infection could be due to an accelerated hyphal growth of individual strains.…”

Section: Discussionmentioning

confidence: 99%

“…Besides, the competitive advantage of individual strain genotypes for transmission is not associated with virulence among the strains (25). The growth of mixed genotypes outside of the host is only poorly associated with the success of the same genotype mix on the plant though (25). The complex links between competitive abilities of the pathogen and consequences for the plant host raise important questions how co-infections impact evolutionary trajectories of host-pathogen systems.…”

Section: Introductionmentioning

confidence: 99%

“…The virulence of co-infecting Podosphaera plantaginis strains can be increased on the Plantago lanceolata host (5). In other systems such as Zymoseptoria tritici infecting wheat, virulence appears unaffected by co-infections (20, 21), however the trajectory of an infection depends on the host genotype and genotypes of competing strains (20, 25). Besides, the competitive advantage of individual strain genotypes for transmission is not associated with virulence among the strains (25).…”

Section: Introductionmentioning

confidence: 99%

“…In other systems such as Zymoseptoria tritici infecting wheat, virulence appears unaffected by co-infections (20, 21), however the trajectory of an infection depends on the host genotype and genotypes of competing strains (20, 25). Besides, the competitive advantage of individual strain genotypes for transmission is not associated with virulence among the strains (25). The growth of mixed genotypes outside of the host is only poorly associated with the success of the same genotype mix on the plant though (25).…”

Section: Introductionmentioning

confidence: 99%

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

Bellah

Seiler

Croll

2022

Preprint

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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 pathogenZymoseptoria 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.

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Section: Discussionmentioning

confidence: 87%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

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

Bellah

Seiler

Croll

2022

Preprint

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Estimating the frequency of virulence against anStbgene inZymoseptoria triticipopulations by bulk phenotyping on checkerboard microcanopies of wheat NILs

Suffert,

Le Prieur,

Gélisse

et al. 2023

Preprint

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Monitoring virulent strains within fungal pathogen populations is crucial to improve host resistance deployment strategies. Such monitoring increasingly involves field pathogenomics studies of molecular polymorphisms in genomes based on high-throughput screening technologies. However, it is not always straightforward to predict virulence phenotypes from these polymorphisms andin plantaphenotyping remains necessary. We developed a method for ‘bulk phenotyping on checkerboard microcanopies of wheat near-isogenic lines’ (BPC) for estimating the frequency of virulence against anStbgene in populations ofZymoseptoria tritici, the causal agent ofSeptoria triticiblotch in wheat, without the need for strain-by-strain phenotyping. Our method involves the uniform inoculation of a microcanopy of two wheat lines – one with the resistance gene and the other without it – with a multi-strain cocktail representative of the population to be characterized, followed by the differential quantification of infection points (lesions). UsingStb16q, a resistance gene that has recently broken down in Europe, we found a robust correlation between the ratio of the mean number of lesions on each wheat line and the frequency of virulent strains in the inoculum. Using pairs of virulent and avirulent strains, and synthetic populations consisting of 10 virulent strains and 10 avirulent strains mixed in different proportions, we validated the principle of the method and established standard curves at virulence frequencies close to those observed in natural conditions. We discuss the potential of this method for virulence monitoring in combination with recently developed molecular methods.

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An array ofZymoseptoria triticieffectors suppress plant immune responses

Thynne,

Ali,

Seong

et al. 2024

Preprint

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Zymoseptoria tritici is the most economically significant fungal pathogen of wheat in Europe. However, despite the importance of this pathogen, the molecular interactions between pathogen and host during infection are not well understood. Herein, we describe the use of two libraries of cloned Z. tritici effectors that were screened to identify effector candidates with putative pathogen associated molecular pattern (PAMP) triggered immunity (PTI)-suppressing activity. The effectors from each library were transiently expressed in Nicotiana benthamiana, and expressing leaves were treated with bacterial or fungal PAMPs to assess the effectors' ability to suppress reactive oxygen species (ROS) production. From these screens, numerous effectors were identified with PTI-suppressing activity. In addition, some effectors were able to suppress cell death responses induced by other Z. tritici secreted proteins. We used structural prediction tools to predict the putative structures of all of the Z. tritici effectors, and used these predictions to examine whether there was enrichment of specific structural signatures among the PTI-suppressing effectors. From among the libraries, multiple members of the killer protein-like 4 (KP4) and killer protein-like 6 (KP6) effector families were identified as PTI-suppressors. This observation is intriguing, as these protein families were previously associated with antimicrobial activity rather than virulence or host manipulation. This data provides mechanistic insight into immune suppression by Z. tritici during infection, and suggests that similar to biotrophic pathogens, this fungus relies on a battery of secreted effectors to suppress host immunity during early phases of colonisation.

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Asexual reproductive potential trumps virulence as a predictor of competitive ability in mixed infections

Cited by 8 publications

References 49 publications

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

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

Estimating the frequency of virulence against anStbgene inZymoseptoria triticipopulations by bulk phenotyping on checkerboard microcanopies of wheat NILs

An array ofZymoseptoria triticieffectors suppress plant immune responses

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