Microbiota-mediated disease resistance in plants

Vannier, Nathan; Agler, Matthew T.; Hacquard, Stéphane

doi:10.1371/journal.ppat.1007740

Cited by 236 publications

(181 citation statements)

References 41 publications

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“…There is a growing body of evidence that commensal microbes interact with the plant immune system. For example, specific strains of Sphingomonas, an abundant, putatively commensal genus in the phyllosphere, stimulate plant immune response 1 , and one can envision that their proliferation is kept in-check by elements of the plant immune system that also control bona fide pathogens 52,53 . In addition, many microbes can probably not easily proliferate in the nutrient-limited conditions of the phyllosphere.…”

Section: The Relationship Between the Presence Of A Single Prolific Tmentioning

confidence: 99%

The relationship between microbial population size and disease in the Arabidopsis thaliana phyllosphere

Karasov

Neumann

Duque‐Jaramillo

et al. 2019

Preprint

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A central goal in microbiome research is to learn what distinguishes a healthy from a dysbiotic microbial community. Shifts in diversity and taxonomic composition are important indicators of dysbiosis, but a full understanding also requires knowledge of absolute microbial biomass. Simultaneous information on both microbiome composition and the quantity of its components can provide insight into microbiome function and disease state. Here we use shotgun metagenomics to simultaneously assess microbiome composition and microbial load in the phyllosphere of wild populations of the plant Arabidopsis thaliana. We find that wild plants vary substantially in the load of colonizing microbes, and that high loads are typically associated with the proliferation of single taxa, with only a few putatively pathogenic taxa achieving high abundances in the field. Our results suggest (i) that the inside of a plant leaf is on average sparsely colonized with an estimated two bacterial genomes per plant genome and an order of magnitude fewer eukaryotic microbial genomes, and (ii) that higher levels of microbial biomass often indicate successful colonization by pathogens. Lastly, our results show that load is a significant explanatory variable for loss of estimated Shannon diversity in phyllosphere microbiomes, implying that reduced diversity may be a significant predictor of microbial dysbiosis in a plant leaf.

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Section: The Relationship Between the Presence Of A Single Prolific Tmentioning

confidence: 99%

The relationship between microbial population size and disease in the Arabidopsis thaliana phyllosphere

Karasov

Neumann

Duque‐Jaramillo

et al. 2019

Preprint

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“…Based on the driver and passenger hypotheses, Hart et al (2001) presented two nonexclusive mechanisms to explain this spatial correlation. Fungal symbionts indeed play a determining role in plant nutrition (Marschner, 1995;Hiruma et al, 2016) and alleviation of environmental stresses (Aug e, 2001;Gange et al, 2005;Vannier et al, 2019). Fungal symbionts indeed play a determining role in plant nutrition (Marschner, 1995;Hiruma et al, 2016) and alleviation of environmental stresses (Aug e, 2001;Gange et al, 2005;Vannier et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Effect of floristic composition and configuration on plant root mycobiota: a landscape transposition at a small scale

et al. 2019

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Fungal communities in the root endosphere are heterogeneous at fine scale. The passenger hypothesis assumes that this heterogeneity is driven by host plant distribution. Plant composition and host plant configuration should then influence root fungal assemblages.We used a large-scale experimental design of 25 mixtures of grassland plants. We sampled Brachypodium pinnatum in each mesocosm, and used amplicon mass-sequencing to analyze the endospheric mycobiota. We used plant distribution maps to assess plant species richness and evenness (heterogeneity of composition), and patch size and the degree of isolation of B. pinnatum (heterogeneity of configuration) on fungal community assembly.The Glomeromycotina community in B. pinnatum roots was not related to either floristic heterogeneity or productivity. For Ascomycota, the composition of operational taxonomic units (OTUs) was driven by plant evenness while OTU richness decreased with plant richness. For Basidiomycota, richness increased with host plant aggregation and connectivity. Plant productivity influenced Ascomycota, inducing a shift in OTU composition and decreasing evenness.Plant heterogeneity modified root mycobiota, with potential direct (i.e. host preference) and indirect (i.e. adaptations to abiotic conditions driven by plant occurrence over time) effects. Plant communities can be envisioned as microlandscapes consisting of a variety of fungal niches.

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“…This paradigm shift increased the complexity of the studied systems and triggered an increase in the use of network approaches in plant pathology. To identify the microorganisms protecting plants against pathogens, several authors suggested considering the statistical associations within meta-barcoding datasets as a proxy for microbial interactions (Poudel et al 2016;Vacher et al 2016;Garett et al 2018;Vannier et al 2019), with the ultimate goal of identifying (groups of) microbial taxa that compete for space or resources with pathogens, parasitizes pathogens or have an antibiosis activity against them (Massart et al 2005, Abdelfattah et al 2018. In this study, we assessed the relevance of this novel line of research using grapevine powdery mildew (Erysiphe necator; Gadoury et al 2012, Armijo et al 2016) as a model system.…”

Section: Discussionmentioning

confidence: 99%

“…The analysis of microbial networks associated with wild relatives of cultivated grapevine or hybrids could also be relevant, given that a recent study highlighted higher abundance of beneficial symbionts in wild vines (Kernaghan et al 2017). Advances in culturomics (Lagier et al 2018) and synthetic microbial communities (Kehe et al 2019;Vannier et al 2019) will also undoubtedly benefit the field of pathobiome research. In the present study, we did a partial validation of the pathobiome network using specific microbial cultures.…”

Section: Discussionmentioning

confidence: 99%

“…A better understanding of plant pathobiomes will allow us to reduce our reliance on chemical pesticides, through the discovery of novel biocontrol agents (Poudel et al 2016) and cultural practices fostering the protective microbiota (Hartman et al 2018). To achieve this aim, research is needed at the interface between plant pathology, microbial community ecology, culturomics, metagenomics and big data (Vannier et al 2019). Culturable and unculturable microorganisms associated with healthy and diseased plants can be described using metabarcoding approaches (Abdelfattah et al 2018;Nilsson et al 2019).…”

Section: Introductionmentioning

confidence: 99%

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Microbial association networks give relevant insights into plant pathobiomes

Pauvert

Fort

Calonnec

et al. 2020

Preprint

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Interactions between plant pathogens and other plant-associated microorganisms regulate disease.Deciphering the networks formed by these interactions, termed pathobiomes, is crucial to disease management. Our aim was to investigate whether microbial association networks inferred from metabarcoding data give relevant insights into pathobiomes, by testing whether inferred associations contain signals of ecological interactions. We used Poisson Lognormal Models to construct microbial association networks from metabarcoding data and then investigated whether some of these associations corresponded to interactions measurable in co-cultures or known in the literature, by using grapevine (Vitis vinifera) and the fungal pathogen causing powdery mildew (Erysiphe necator) as a model system. Our model suggested that the pathogen species was associated with 23 other fungal species, forming its putative pathobiome. These associations were not known as interactions in the literature, but one of them was confirmed by our co-culture experiments. The yeast Buckleyzyma aurantiaca impeded pathogen growth and reproduction, in line with the negative association found in the microbial network. Co-cultures also supported another association involving two yeast species. Together, these findings indicate that microbial networks can provide plausible hypotheses of ecological interactions that could be used to develop microbiome-based strategies for crop protection. Pauvert et al. 2020. Pathobiome networks 3

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Microbiota-mediated disease resistance in plants

Cited by 236 publications

References 41 publications

The relationship between microbial population size and disease in the Arabidopsis thaliana phyllosphere

The relationship between microbial population size and disease in the Arabidopsis thaliana phyllosphere

Effect of floristic composition and configuration on plant root mycobiota: a landscape transposition at a small scale

Microbial association networks give relevant insights into plant pathobiomes

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